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PART 3
WILDLIFE FAUNA AND
INTEGRATION OF ORGANIC
MATTER INTO MARINE FOOD WEBS
TASK 10
VERTEBRATE FOOD WEBS
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Task 10:
Vertebrate Food web
Costa, M.J.; Catarino, F.; Salgado, J.P.; Serôdio, J.; Cabral, H. &
Franco, M.A.
Final Report
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Lisbon, Portugal 2000
1 ABSTRACT
2 INTRODUCTION
3 PRIMARY PRODUCTION
3.1 Identification of the main sources of organic matter
3.1.1 Introduction
3.1.2 Methodology
3.1.3 Results
3.2 Mycrophitobenthos production
3.2.1 Introduction
3.2.2 Methodology
3.2.3 Modelling
3.2.4 Results
3.2.5 Discussion
3.2.6 References
4 SECONDARY PRODUCTION
4.1 Benthic meiofauna
4.1.1 Introduction
4.1.2 Methodology
Study area
Sampling
Sediment analysis
Meiobenthos analysis
Data analysis
4.1.3 Results
4.1.4 Discussion
4.2 Benthic Macrofauna
4.2.1 Sampling sites
4.2.2 Methodology
Sediment analysis
4.2.3 Results
Sediment analysis
Species composition
Seasonal Analysis
Specific richness , diversity and evenness
4.3 Fish assemblages in tidal salt marsh creeks and in adjoining mudflat areas in Tagus estuary
4.3.1 Introduction
4.3.2 Methodology
Study Area
Data analysis
4.3.3 Results
Abiotic conditions
Community structure
Seasonal variation
4.3.4 Discussion
5 TROPHIC ANALYSIS
5.1 Food habits of Pomatoschistus microps (Krøyer , 1838) in the Tagus salt marsh
5.1.1 Introduction
5.1.2 Methodology
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5.1.3 Results
5.1.4 Discussion
5.2 Food habits of Liza ramada (Risso, 1826) in the Tagus salt marsh
5.2.1 Introduction
5.2.2 Methods
5.2.3 Results and discussion
5.3 Isotope analysis
5.3.1 Methods
5.3.2 Results
5.4 Food web
6 REFERENCES
7 PUBLICATIONS
1
ABSTRACT
In the latest projects “Comparative studies of salt marsh processes” and “effects of
environmental change on European salt marshes” our team investigated the structure and
functioning of the food web from the salt marsh surrounding areas of the Mira and Tagus
estuaries and compared them.
In the follow up of the latest projects, EUROSAM, we pretend to study the Tagus estuary
vertebrate food web within the different salt marsh compartments, such as mudflats, creeks and
vegetation cover areas, to understand the importance of the direct usage of those habitats by the
fish community. However studies in these areas are scarce and there is no information on the
aquatic fauna present in these salt marshes. For that purpose first we identified quantitative and
qualitative trends in the fish, decapod crustaceans and benthic meio and macroinvertebrates
communities and we estimated the primary productivity rates of intertidal microphytobenthos of
the Tagus estuary. After choosing k-species we followed-up the food web from the lowest levels,
identifying and characterising the main potential sources of organic matter, to the highest ones.
When considering the entire intertidal area of the Tagus estuary, microphytobenthic primary
production was estimated to attain 4265.1 ton C yr
-1
.
Detritivorous and benthic invertebrate feeders dominate the higher levels of the food web in the
salt marsh tidal creeks. The major difference between the salt marsh and the adjoining area food
webs is the absence or presence in lower abundance’s of crabs and several fish species, as the
ell, the sea bass, the sand goby and the soles. Some of those species are potential predators of
small size fish. Thus, young of the year of several fish species feeding in the salt marsh areas
decrease the risk of being preyed by other fish species.
The use of the tidal creeks as feeding grounds by a high fish biomass suggest the important roll
of these taxa in the organic matter transport processes between the salt marsh and the adjoining
areas.
Part of the results of this task are presented in one Ph.D. Thesis (Serôdio 1999) and in two
articles submitted for publication (Serôdio et al. and Salgado et al.).
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2
INTRODUCTION
In the latest projects “Comparative studies of salt marsh processes” and “effects of
environmental change on European salt marshes” our team investigated the structure and
functioning of the food web from the salt marsh surrounding areas of the Mira and Tagus
estuaries and compared them.
In the follow up of the latest projects we pretend to study the Tagus estuary vertebrate food web
within the different salt marsh compartments, such as mudflats, creeks and vegetation cover
areas, to understand the importance of the direct usage of those habitats by the fish community.
However studies in these areas are scarce and there is no information on the aquatic fauna
present in these salt marshes. For that purpose first we identified quantitative and qualitative
trends in the fish, decapod crustaceans and benthic invertebrates communities and we
estimated the primary productivity rates of intertidal microphytobenthos of the Tagus estuary.
After choosing k-species we followed-up the food web from the lowest levels, identifying and
characterising the main potential sources of organic matter, to the highest ones.
Part of the results of this task are presented in one Ph.D. Thesis (Serôdio 1999) and two article
submitted for publication (Serôdio et al. submitted and Salgado et al.) included as annexes.
3
PRIMARY PRODUCTION
3.1
Identification of the main sources of organic matter
3.1.1
Introduction
The main goal of this study is to identify the main sources of organic matter for the aquatic
consumers in salt marsh and contiguous mudflat of the upper Tagus estuary.
For that purpose we determined the C, S and N isotopic relative abundances of the main primary
producers and the amount of chlorophyll a (Chl a), suspended particulate matter (SPM) and
particulate organic matter (POM) in several areas of the estuary.
Stable isotopes values of POM and of the filter feeder Scrobicularia plana were analysed. POM
isotopic values represent the spatial variability of both plant detritus and phytoplancton,
suspended in the water column. Isotope values of S. plana are a signal of the POM that is
assimilated.
3.1.2
Methodology
The macrophytes Spartina maritima, Arthrocnemon fruticosum and Halimione portulacoides were
sampled during Spring in Hortas and Vasa sacos creeks. Water samples for Chl a, SPM and
POM analysis were collected also during Spring at high tide inside both tidal creeks in the nearby
subtidal areas and in the middle of the estuary and at low tide in three tributaries of the estuary
(V. F. de Xira in the Tagus river, Porto alto in the Sorraia river and Ponte in the Enguias stream)
. These water samples were stored in dark until filtration in the laboratory was done. Water
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samples for POM isotope analyses were vacuum filtered until clogged onto precombusted filters.
Individuals of S. plana for isotope analysis were collected from the mouth of both tidal creeks.
Samples for analysis of multiple stable isotopes were processed following the sample preparation
guidelines of the Stable Isotope Laboratory, Ecosystem Center, MBL (MA, USA).
Tissues of macrophyte species were cleaned of mud and when present, epiphytes were removed
by scraping with a razor blade. Samples were then dried to constant weight at 60 ºC. The dried
tissues were ground to a fine powder with a mortar and a pestle. Plant tissue samples for
13
C
were checked for contamination by carbonates. Subsamples of the ground sample were acidified
with several drops of 10% HCl while being observed under a dissecting microscope. If bubbling
occurred the whole sample was acidified, redried at 60 ºC and stored in glass vials. Plant tissue
samples for
34
S were ground and rinsed in deionised water to remove seawater sulphate
(resuspended in deionised water, centrifuged for 5 min, and supernatant discarded; this
procedure was repeated three times), redried at 60 ºC and stored in glass vials.
Animal tissue samples for C, N and S stable isotope analysis were dissected to isolate muscle
tissue and were dried at 60 ºC. The dried tissues were ground to fine powder with a mortar and a
pestle. Ground animal
13
C tissue samples, suspected of having carbonate contamination, were
acidified with 10% HCl and redried at 60 ºC. Ground animal tissue samples for
34
S rinsed in
deionised water to remove seawater sulphate and redried at 60 ºC.
Each isotope analysis of a species represented a subsample from a pooled sample of several
individuals. This was done to minimise the variability associated with analysis of different
individual organisms and to gain enough material for S isotope analysis.
Chl a was measured using the methodology presented by Lorenzen (1967).
3.1.3
Results
Due to problems in the mass spectrometer that is running the samples for the stable isotope
analysis it is not possible yet to present any results on these parameters. However we expect to
have them at any moment. More samples for this part of the work were collected in the beginning
of junne and are still being analysed. Nevertheless, here we present the results of the spatial
distribution of suspended particulate matter (SPM), particulate organic matter (POM) and
chlorophyll a (Chl a) in surface waters of Tagus estuary (table I).
Table I - Spatial distribution of suspended particulate matter (SPM), particulate organic matter
(POM) and chlorophyll a (Chl a) in surface waters of Tagus estuary
Stations
SPM
(g.m
-3
)
POM
(g.m
-3
)
Chl a
(g.m
-3
)
VFX
30.0
12.0
3.2
A
33.0
13.2
1.6
Pa
90.5
21.0
1.7
H
178.8
48.7
8.7
Vs
51.0
17.7
4.4
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3.2
Mycrophitobenthos production
3.2.1
Introduction
The primary production of intertidal microphytobenthos of the Tagus estuary, Portugal, was
quantifyied through the formulation of a simulation model. The variables used as forcing
functions in the model, in situ irradiance, productive biomass and P vs. E curve parameters a
and P
m
, were measured with hourly resolution. The model was used for comparing the variability
in production on hourly (intraday), fortnightly (within spring-neap tidal cycles) and seasonal
(month-to-month) time scales. The model allowed for the prediction of hourly production rates for
the whole year and for the estimation of annual primary production of the Tagus estuary.
3.2.2
Methodology
Primary productivity rates of intertidal microphytobenthos of the Tagus estuary were estimated
from in situ time series of measurements of photosynthetic active radiation (PAR) and
temperature and from photosynthesis versus irradiance (P-I) curves measured at different times
during low tide periods.
Sampling was carried out in an extensive intertidal mudflat located near Pancas salt marsh, on
the south margin of the Tagus estuary, Portugal. The sampling site was representative of the
intertidal areas of the estuary, being composed of fine muddy sediment, with 90.6% of particle
sizes below 20 µm, and colonised by microphytobenthic communities typically dominated by
diatoms (Brotas and Plante-Cuny 1998). Sediment samples were collected during low tide using
plexiglas corers (1.9 cm internal diameter) and taken to the laboratory where were placed
outside, in an artificial tidal system which simulated the immersion during high tide using
estuarine water collected on the day of sediment sampling.
During three spring-neap tidal cycles, photosynthetically active radiation (PAR, 400-700 nm) was
measured continuously at the sediment surface at the sampling site, using an underwater
quantum sensor (LI-192SA, LI-COR, Nebraska, Lincoln, USA) connected to a data logger (Delta-
T Logger, Delta-T Devices, Cambridge, UK), positioned ca. 10 cm above the sediment surface.
Primary production was determined by measuring gross oxygen photosynthetic production, using
Clark type oxygen microelectrodes (5-20 µm tip 737-GC model, Diamond General) according to
Revsbech and Jørgensen (1983). The microelectrode was positioned vertically within the
sediment using a micromanipulator and was connected to a picoammeter (model 8100
Electrometer, Keithley Instruments, Cleveland, Ohio, USA). Photosynthesis was measured at
depth intervals of 50 µm and then integrated over all depth intervals to yield the community
photosynthetic rate. P-I curves were constructed by exposing the same sediment core to eight
different incident irradiance levels and measuring the community photosynthetic rate under each
level.
Productive biomass was estimated by measuring dark-level Chl a fluorescence, Fo, using a
pulse amplitude modulation fluorometer (PAM 101 Chlorophyll Fluorometer, Heinz Walz,
Effeltrich, Germany). The PAM fiberoptics was positioned perpendicularly to the sediment
surface, at a fixed distance of 1 mm, and readings were considered after signal stabilisation
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following darkening of the sample. The relative positions of the sample surface, the fiberoptics
and the oxygen microelectrode were set with the help of a micromanipulator (MM33, Diamond
General, Ann Arbor, Michigan, USA) to which the corer was attached.
3.2.3
Modelling
The patterns of variation of PAR and productive biomass were used as forcing functions in the
calculation of annual primary production rates of intertidal microphytobenthos for different tidal
heights. A linear relationship between productive biomass and P-I curve parameters was used to
estimate photosynthetic rate at each point in time and for different tidal heights. F
o
was used to
predict short-term variations in the community photosynthetic light response, by quantitatively
relating F
o
to P vs. E curve parameters.
Based on the in situ measurements of the irradiance level reaching the sediment surface during
whole spring-neap tidal cycles (Serôdio & Catarino 1999), the model was run considering that
during high tide the irradiance at the sediment surface was null.
Since the relationship between F
o
and the P vs. E curve parameters allows for the direct
estimation of hourly production rates from F
o
and E observations, the estimation of annual
production budgets was approached through the modelling of the F
o
variability throughout an
entire annual period. The model used for describing the hourly variation of F
o
is a modification of
the model formulated by Pinckney & Zingmark (1991).
The relationship between F
o
and a and between F
o
and P
m
was quantitatively defined by
calculating the slope and the y-intercept of linear regression equations fitted to paired
measurements of F
o
and a and of F
o
and P
m
.
3.2.4
Results
PAR reaching the surface of intertidal sediments was strongly conditioned by the periodic tidal
inundation, with large and abrupt variations occurring during flooding and ebbing (Fig. 1). PAR
levels decreased very rapidly to null or very low values with the incoming of the tide during most
of the daytime immersion periods. Only on neap tides, when the water column during high tide is
lower, some light reached the sediment surface. The variation of the time of day of tidal emersion
along the Spring-neap tidal cycle resulted in a clear fortnightly variation in total daily PAR
reaching the sediment surface. Maximum daily PAR values were recorded on the days when
tidal inundation occurred at the beginning and at the end of the day, which coincides with the
days preceding the neap tides. Minimum values were observed on the days preceding the Spring
tides, in which tidal inundation occurs during the middle of the day.
The photosynthetic light response was also found to vary significantly, mainly on hourly time
scale (Fig. 2). This variability was shown to result mainly from rapid and substantial changes in
productive biomass, caused by vertical rhythmic migration of motile diatom cells (Serôdio et al.,
1997).
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A linear relationship was found between F
o
and P vs. E curve parameters a and P
m
, either when
considering each fortnight period separately or when pooling the data from the three periods.
Highly significant regression equations were found in all cases when a and P
m
were regressed
against F
o
.
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Figure 1 - Example of PAR (filled area) and temperature (line) variability at the surface of
intertidal sediment during on Spring-neap tidal cycle. Horizontal bars and vertical
dotted lines mark the high tide periods.
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Figure 2 - Typical short-term variation photosynthetic light response of undisturbed
microphytobenthos.
As a result of high variability in both incident PAR and community photosynthetic efficiency,
primary production rates were found to vary considerably on hourly and fortnightly time scales,
resulting in an annual pattern of daily primary production characterised by a strong fortnightly
quasi-cyclic variability superimposed on an underlying seasonal trend (Fig. 3).
Figure 3 - Model-predicted annual variation of mean daily production rate.
In general, maximum hourly production rates were obtained near neap tides, during days when
the low tide exposure occurred near the middle of the day, and minimum rates near Spring tides,
when the opposite situation occurred. Spatially, microphytobenthic primary production was
predicted to increasing with tidal height, which determines the number and extent of exposure
during low tide and, hence, the annual amount of light available for photosynthesis.
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When the model was run for 4 different years, the pattern of daily production was essentially the
same and the estimates of annual production varied by less than 7%. For this 4-year period,
annual areal production ranged from 12.47 to 13.34 mol O
2
m
-2
yr
-1
or, converting oxygen
production (mol O
2
) to carbon assimilation (g C) assuming a 1:12 ratio (Cammen 1991,
Pinckney & Zingmark 1993a), from 149.6 to 160.1 g C m
-2
yr
-1
. The estimation of the annual
primary production of the entire intertidal area of the Tagus estuary was approached by running
the model for the whole range of tidal heights (from 0.1 m to 4.1 m, at 0.1 m intervals) and by
extrapolating the annual areal production values calculated for each tidal height for the total
intertidal area corresponding to the same tidal height interval. For each tidal height interval, the
total intertidal area was calculated from average heights of 300 m x 300 m areas computed from
bathymetry charts for the Tagus estuary. From the annual areal primary production rate
predicted for each tidal height interval, an annual production map for the intertidal areas of the
Tagus estuary was constructed (Fig. 4). For the total 114.48 km
2
of intertidal area of the Tagus
estuary, mean annual primary production was estimated to reach 4265.1 ton C yr
-1
.
3.2.5
Discussion
The interference between the tidal and the day/night cycles cause the estuarine intertidal
environment to be dominated by strong variability in a number of different time scales. The use
of a sampling design of this type allowed for the finding that microphytobenthic primary
productivity is dominated by variability on sub-seasonal (hourly and fortnightly) time scales.
These results have important consequences for the design of sampling programs for the
characterization of the temporal patterns of variation of microphytobenthic productivity, as the
usual practice of measuring production monthly throughout the year does not provide information
on the within-month variability and may yield erroneous seasonal pattern due to liasing.
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Figure 4 - Estimated spatial distribution of microphytobenthic annual primary production for the
entire intertidal area of the Tagus estuary.
The predominance of fortnightly over seasonal variability in microphytobenthic productivity
predicted for the Tagus estuary is not likely to be a generalised feature of estuarine ecosystems,
as it is determined by factors associated to the particular geographic location of each estuary. In
general, seasonality is expected to increase with latitude, following the higher month-to-month
variations in irradiance and temperature, as shown in a recent comparison of results from
different estuaries (MacIntyre et al., 1996). In the Tagus estuary, the fortnightly variability in daily
production is caused by the variation in the daily available irradiance along the Spring-neap tidal
cycle: during Spring tides, low tide occurs early in the morning and late in the afternoon;
conversely, during neap tides, low tide occurs in the middle of the day. In other estuaries,
different tidal regimes and less turbid water may reduce the relative importance of the Spring-
neap cycle on benthic production.
The coincidence of maximum daily production rates with minimum resuspension of benthic
biomass during neap tides (considering the tidal amplitude as an indicator of the resuspension
intensity) is likely to cause a marked fortnightly variability in the availability of microphytobenthic
biomass for the estuarine food web. In the period between Spring and neap tides, the
simultaneous increase in daily production and decrease in resuspension intensity favours the
accumulation of microphytobenthic biomass on the tidal flats, but at the same time a reduction in
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the transfer of benthic biomass for the pelagic food web. On the opposite phase of the Spring-
neap cycle, while biomass on the tidal flats is expected to decrease following to the reduction of
daily production and the increase in resuspension rates, the availability of benthic microalgae for
filter feeders or benthic grazers on other areas of the estuary is expected to increase. Such a
process would contribute to attenuate the impact of the fortnightly variation in intertidal primary
production at the ecosystem-level primary and secondary productivity.
Considering the interannual variation in the annual estimates, a maximum range of 149.6 - 160.1
g C m
-2
yr
-1
and a mean value of 155.8 g C m
-2
yr
-1
are obtained for the annual areal production
rate of the studied intertidal microphytobenthos of the Tagus estuary. These values are within
the range of estimates reported for other estuaries (for a recent review, see MacIntyre et al.,
1996), and close to previous estimates made for this estuary. Based on measurements of
community net photosynthesis, Brotas & Catarino (1995) estimated annual production as 47 and
178 g C m
-2
yr
-1
, values calculated for sites at tidal heights of 1.4 m and 3.1 m, respectively.
The use of different methodologies to measure microphytobenthic photosynthesis and the
different methods used to extrapolate from hourly to annual production rates, makes difficult a
direct comparison between the estimates obtained in both studies. However, when the present
model is run for the tidal height of 3.1 m, and the resulting estimate is converted to net
production (80% of gross production, value estimated for similar microphytobenthos
communities in the Tagus estuary), a mean value of 164.9 g C m
-2
yr
-1
is obtained, 7.3% lower
than the estimate of Brotas & Catarino (1995).
Because the model was not validated for tidal heights or locations other than the used for
estimating its parameters, some caution must be used in the analysis of the results obtained
concerning the estimation of annual production rate for the whole estuary. The main causes for
failure in the model predictions are the variation in the fraction of microalgae that are motile and
overall biomass, which are usually lower in sandier sediments, and the effects of desiccation on
sites that are not inundated during neap tides (tidal height above 2.9 m). Also variations over
space in the community physiological light response, associated to differences in taxonomic
composition or to photoacclimation to different light regimes, may contribute for errors in the
model predictions.
The annual gross primary production for the whole intertidal area of the Tagus estuary
estimated by taking into considerationthe representativenessof the different tidal heights
and the production estimated for each tidal height interval, 4265.1 ton C yr
-1
, was
substantially different from the value obtained by directly extrapolating the areal
production rate estimated at a single tidal height for the entire intertidal area, 17858.9 ton
C yr
-1
. This highlights the importance of the development and validation of improved
production models that consider the variability of production rates with tidal height in the
estimation of ecosystem-level production.
3.2.6
References
Brotas V, Catarino F (1995) Microphytobenthos primary production of Tagus estuary intertidal
flats (Portugal). Netherlands Journal of Aquatic Ecology 19:333-339.
Brotas, V. & M. R. Plante-Cuny (1998) Spatial and temporal patterns of microphytobenthic taxa
of estuarine tidal flats in the Tagus Estuary (Portugal) using pigment analysis by HPLC.
Marine Ecology Progress Series 171: 43-57.
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Cammen LM (1991) Annual bacterial production in relation to benthic microalgal production and
sediment oxygen uptake in an intertidal sandflat and an intertidal mudflat. Marine Ecology
Progress Series 71:13-25.
MacIntyre HL, Geider RJ, Miller DC (1996) Microphytobenthos: The ecological role of the “secret
garden” of unvegetated, shallow-water marine habitats. I. Distribution, abundance and
primary production. Estuaries 19:186-201.
Pinckney J, Zingmark RG (1991) Effects of tidal stage and sun angles on intertidal benthic
microalgal productivity. Marine Ecology Progress Series 76:81-89.
Pinckney JL, Zingmark RG (1993) Modelling the annual production of intertidal benthic
microalgae in estuarine ecosystems. Journal of Phycology 29:396-407.
Revsbech, NP & BB Jørgensen. 1983. Photosynthesis of benthic microflora measured with high
spatial resolution by the oxygen microprofile method: Capabilities and limitations of the
method. Limnology and Oceanography 28: 749-756.
Serôdio J 1999 Modelling the primary productivity of intertidal microphytobenthos. Role of
migratory rhythms studied by in vivo chlorophyll fluorescence. University of Lisbon, 168 p.
Serôdio J, Catarino F 1999 Fortnightly light and temperature variability in estuarine intertidal
sediments and implications for microphytobenthos primary productivity. Aquatic Ecology
33:235-241.
Serôdio J, Marques da Silva J & Catarino F 1997 Nondestructive tracing of migratory rhythms of
intertidal microalgae using in vivo chlorophyll a fluorescence. Journal of Phycology 33:542-53.
Serôdio J, Marques da Silva J & Catarino F. Use of in vivo chlorophyll a fluorescence to quantify
short-term variations in the productive biomass of intertidal microphytobethos. Submited for
publication.
4
SECONDARY PRODUCTION
4.1
Benthic meiofauna
4.1.1
Introduction
The importance of meiofauna in the estuaries is very high and according to Coull (1999) it plays
a role in three fields: it facilitates biomineralization, feeds various higher trophic levels and show
a high sensibility to antropogenic actions, making them excellent organisms for estuarine
pollution biomonitoring.
According to Heip et al. (1992) the latitude has influence on the meiobenthic communities;
therefore the majority of studies have been conducted at latitudes different from the Tagus
estuary latitude, mainly in Northern Europe (e.g. Merilaeinen, 1988; Escravage et al., 1989;
Vanreusel, 1991; Heip et al., 1992; Steyaert & Vincx, 1996; Moodley et al., 1998a; Blome et al.,
1999) and in Southern EUA (e.g. Bell, 1979; Fleeger et al., 1982; Montagna et al., 1983; Coull,
1985; Coull, 1999).
Meiofauna are badly known in Southern Europe estuaries. In Portugal their knowledge is limited
to the work of Rosado & Bruxelas (1995), Rosado (1996), Adão & Marques (1999) and Austen et
al. (1989). In Tagus estuary there is only a study comparing the communities in several
European estuaries (Heip & Herman, 1995). In this work only four sites were sampled in a single
season (Soetaert et al., 1995).
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Meiofauna are characterised by high densities (between 10
5
e 10
7
ind m
-2
) (Coull, 1999). In
temperate estuaries this group is dominated by nematodes and followed generally by copepods
(Heip et al., 1990; Heip et al., 1995), although there may be significant differences in sub-
dominant groups (Soetaert et al., 1995). Spatial distribution of meiofauna in sediment follows an
aggregated pattern (Fleeger et al., 1990; Steyert et al., 1999) both horizontally and vertically.
Although this is a complex issue since environmental gradients are sharper vertically, it is also in
this direction that fauna and flora show a strong vertical zonation (Joint et al., 1982).
The processes that generate and maintain the vertical distribution pattern in different places are
scarcely known and according to Steyaert et al. (1999) they are an important challenge for
modern ecology research.
In temperate zones, tidal and shallow subtidal meiofauna typically shows a seasonal pattern
(Smol et al., 1994). According to Coull (1999) this seasonality is directly or indirectly related to
temperature pattern by means of factors induced by it. According to the same author (1985) other
biological processes may also have a bear on meiofauna seasonality.
Although other groups such as microphytobenthos (Brotas, 1995, Brotas et al., 1995),
macrofauna (Calvário, 1982; Costa et al., 1996; Costa et al., 1999), ichthyofauna (Costa, 1982;
Costa et al., 1996; Cabral, 1998) and birds (Moreira, 1995), are relatively well studied in the
Tagus estuary, the knowledge of meiofauna is practically non existent.
For a better understanding of meiobenthic community in the Tagus estuary we intend to
establish their composition in terms of great taxonomic groups, their vertical distribution pattern
and their variation in time.
4.1.2
Methodology
Study area
The Tagus estuary on the Portuguese Western coast (38°44’N, 9°08’W) is the largest
Portuguese estuary and one of the largest estuaries in Europe. It covers an approximate area of
320 Km
2
, where 40% are tidal areas (Bettencourt, 1979) made up basically of sand and mud
flats and some salt marshes. The largest area of the tidal platforms is on the Southern margin.
In the Tagus estuary the tides are semi-diurnal with amplitudes higher than in the ocean, varying
from 2 to 4,6m (Costa, 1999).
The salinity of an average high tide varies from typical values of 36‰ in the coastal zone to
27‰ in the widest part of the estuary, with a quick decreasing gradient upstream with values of
0,5‰ 50km from the mouth of the river. In low tide the values at the mouth of the river are
30-33‰ , maintaining the sharp gradient from the widest part of the estuary up to Vila Franca de
Xira (Costa, 1999).
The temperature amplitude is also higher in the estuary than in the ocean, with a highest
amplitude in the upper zones of the estuary (Bettencourt, 1979).
The sampling sites are on the Southern margin near Alcochete (Fig. 5)
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Figure 5 - Tagus estuary map showing the sampling sites (square). The tidal areas are shown in
brown.
Two sampling sites were chosen in the tidal zone: Hortas and Eucaliptal. The first site, Hortas, is
a mud flat with a salt marsh on one side and a small water channel, Ribeira das Enguias, on the
other side. The sediment is muddy and is little disturbed by man since it is a difficult place to
reach, even though it is common to observe in low tide high concentrations of birds feeding in
that area, what causes some disturbance to the sediment.
The other sampling site, Eucaliptal, is an area located on the other margin of Ribeira das
Enguias, and is very easy to reach. The sediment is more heterogeneous and sandier. Is a
preferential place for placing boats and catching clams and crabs, and so it is more disturbed by
man.
Sampling
Six cores were taken in each sampling site, using a piston-style core with a 3.57cm inner
diameter and buried 10cm deep, according to Fleeger et al. (1988), Thiestle & Fleeger (1988)
and Soetaert et al. (1994). The 6 cores comprehend 2 replicates taken in 3 different spots, one
replicate for determining the meiobenthic community and the other for the analysis of chlorophyll
a and pheopigments analysis. Two cores seem to be the minimum accepted for analysing the
meiobenthic community; 3 cores are accepted as an adequate number of cores for this kind of
study (Bouwman, 1987; Steyaert com. pess.).
Each core was cut in four layers, 0-1cm, 1-3cm, 3-6cm and 6-10cm. In each site, sediment
samples were also taken to determine the granulometry, water content and organic matter
content in the sediment. These samples were also cut in the same layers mentioned above.
Samples were taken in Summer and Autumn.
The identification of the samples includes two letters and one number: the first letter refers to the
sampling site, H to Hortas and E to Eucaliptal; the second letter refers to the season, S to
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Summer and A to Autumn; the number indicates the layer, 1 for the first layer (0-1cm), 2 for the
second (1-3cm), 3 for the third (3-6cm) and 4 for the fourth (6-10cm).
Sediment analysis
The samples for granulometry were dried at 60ºC for 24h. About 100g dry weight were washed in
a 63µm sieve to wash out the mud. The sediment retained in the sieve was dried again at 60ºC
for 24h and passed through two sieves of 2mm and 63µm mesh. The sediment retained and
centrifuged in each sieve was then weighted to determine the mud content (the part smaller than
63µm), the sand content (the fraction smaller than 2mm but bigger than 63µm) and the gravel
content (the fraction bigger than 2mm).
Water content was assessed by drying the samples at 60ºC for 24 hours while the total organic
matter was determined after destruction in a muffle furnace (2h at 450ºC).
The pigments, chlorophyll a and pheopigments were extracted with 90% Acetone for 24h in dark
at 4ºC, and then centrifuged. The chlorophyll a, normally used, as an indicator of the
microphytobenthos biomass, and the pheopigments concentration was determined with a
spectrophotometer, accordingly to the methodology presented by Lorenzen (1967). The pigment
concentration was expressed in µg/g of dry sediment.
Meiobenthos analysis
The sediment samples for the determination of the meiobenthic community were placed in plastic
bottles identified and fixed with a 4% formaldehyde solution neutralised with Borax (Pfannkuche
& Thiel, 1988).
The sediment was then washed through two sieves with a 1mm and 38µm mesh and the
sediment in the 38µm sieve was centrifuged in a LUDOX HS-40. Each sample was centrifuged
three times for 10 min, at 2600rpm, in 400ml recipients. The meiofauna retained in the
supernatant was removed after each centrifuge. Finally all meiofauna was keep in a 4%
formaldehyde solution neutralised with Borax and stained wit Bengal rose.
The organisms were classified in the main taxonomic groups and counted with binocular and/or
microscope. The densities of each group were calculated. The density unit most used is the
number of individuals per 10cm
2
of the sediment surface. This unit is used to compare equal
sediment volumes; since in this work the sediment volume of each layer is different, the unit
used was the number of individuals per 10cm
3
. When the whole core is considered and
compared with the other cores the volume is the same and then the unit used was ind/10cm
2
,
which allows the values to be compared with data of other studies.
Data analysis
The community structure was evaluated through a correspondence analysis, using the CANOCO
(4.0 version) program. The groups with a low occurrence (present in less then 10 of the 48
samples) were excluded (i.e. Bivalvia, Gastropoda, Isopoda, Tardigrada and Insecta). The data
referring to water, organic matter and mud content, and the chlorophyll a and pheopigments
concentration were included as co-variables.
4.1.3
Results
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The values of the water, organic matter and mud content in the sediment are shown in table I.
Since the gravel content was not relevant, table I only shows the value of the mud content, the
other being the sand content. In Hortas, the mud content was always higher than 99%. In
Eucaliptal, the sediment was sandier, especially in Autumn when it varied from mud in the first
layers to sand in the fourth layer.
In general a decrease of the water and organic matter content decreased with depth.
Table I – Percentage of water (WC), organic matter (OM) and mud content in the sediment for
the two sampling sites in Summer and Autumn.
Station
Layer
WC
OM
Mud
HS
1
49
7,1
99,7
2
44
6,7
99,8
3
47
6,9
99,8
4
46
6,9
99,6
ES
1
56
8,4
89,3
2
55
8,4
91,1
3
51
8,6
91,2
4
44
7,6
87,6
HA
1
64
8,4
99,4
2
54
7,9
99,7
3
51
7,9
99,6
4
47
8,0
99,5
EA
1
54
8,5
85,6
2
49
5,5
58,3
3
34
4,0
43,0
4
30
4,0
36,0
The values of chlorophyll a and pheopigments concentration in the sediment and the chlorophyll
a / pheopigments ratio are shown in figure 6.
a b c
d
Figure 6 - Mean values of chlorophyll a and pheopigments concentration in the sediment and
chlorophyll a / pheopigments ratio at the two sampling sites in Summer and Autumn. (a
– Hortas in Summer; b – Eucaliptal in Summer; c - Hortas in Autumn; d – Eucaliptal in
Autumn).
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In general the values of chlorophyll a and pheopigments concentration reached their maximum in
the first layer and decreased with depth. Higher values of chlorophyll a were observed in
Autumn.
The pheopigments presented higher values than chlorophyll a. In Hortas these values were
higher in Summer than in Autumn, while in Eucaliptal the values related to Autumn were higher
in the first layers and lower in the deepest layers.
The chlorophyll a / pheopigments ratio was higher in the first layers and decreased with depth.
This ratio increased from Summer to Autumn.
From the groups considered by Higgins & Thiel (1988) the following taxa were identified in the
samples collected in Hortas and Eucaliptal: Sarcomastigophora, Ciliophora, Turbellaria,
Nematoda, Rotifera, Polychaeta, Oligochaeta, Tardigrada, Ostracoda, Copepoda, Isopoda,
Halacaroidea, Insecta, Gastropoda e Bivalvia. Nauplii of crustaceans were also found in great
quantities and although they do not represent a taxonomic group they were also included in this
study.
Taking into account all the samples observed, the meiofauna density varied from 0,3 to 438,2
individuals per cm
3
of sediment. The density and diversity of taxonomic groups were greater in
the first layers, decreasing with depth. The densities of the meiobenthic groups are shown in
figure 7.
Figure 7 - Mean density values of the meiobenthic groups considered at the two sampling sites
in Summer and Autumn.
As regards the vertical distribution and the dominant groups, there was a clear difference
between the two seasons. In Summer more than 90% of the individuals were found in the two
first layers, from which 69% (Hortas) and 76% (Eucaliptal were on the first layer (fig. 8). In
Autumn the individuals had a deeper distribution, reaching 90% only in the third layers.
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Figure 8 - Mean percentage of individual in each layer and respective mean density value (ind/
cm
3
) at the two sampling sites in Summer and Autumn.
The dominance of the different groups is shown in figure 9. The Nematoda were always the
dominant group in the first three layers. In Summer for both sites the dominant group was the
Sarcomastigophora, while in Autumn the Nematoda group continued to be dominant, at both
sampling sites.
Figure 9 - Relative mean percentage of the meiobenthic groups considered in each layer in
Summer and Autumn at the two sampling sites.
In Summer the diversity was lower than in Autumn. Only the groups Nematoda, Copepoda,
Sarcomastigophora and the crustacean nauplii presented high densities, while in Autumn the
groups Rotifera, Turbellaria and Ciliophora presented high densities too.
In general at Eucaliptal the densities were higher than at Hortas, and there was an increase of
the meiobenthic density from Summer to Autumn although this increase was not as clear in
Eucaliptal (48%) as in Hortas (76%) (Fig. 10).
Figure 10 – Mean density (ind/10cm
2
) of the meiobenthic groups per core at the two sampling
sites, in Summer and Autumn. The value of that mean density for the group
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Nematoda is also indicated in the figure together with the percentage of Nematoda
in relation to the total individual number.
The density of the groups Nematoda, Copepoda, Polychaeta, Oligochaeta and Ostracoda and
also the crustacean’s nauplii increased from Summer to Autumn. The groups Rotifera,
Turbellaria and Ciliophora occurred almost exclusively in Autumn. The density of the group
Sarcomastigophora decreased from Summer to Autumn. Although the density of the group
Bivalvia apparently increased from Summer to Autumn, and the groups Gastropoda, Insecta,
Isopoda and Tardigrada only occurred in Autumn, these groups presented very low densities
which did not make it possible to establish a pattern.
The results of the correspondence analysis are shown in table II and figure 11.
Table II – Eigen values and variance cumulative percentage.
Axes
1
2
3
4
Total
inertia
Eigen values
0.516
0.377
0.176
0.142
1.511
Species-environmental correlation
0.774
0.687
0.345
0.373
Species
variance
cumulative
percentage
34,1
59,1
70,7
80,1
Species-environment
variance
cumulative percentage
53,3
84,0
87,7
91,1
The two first factorial axes explain 59% of the variance related to the meiobenthic groups and
84% resulting from the relation between these groups and the environmental variables
considered.
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Figure 11 – Top: Representation of the meiobenthic groups in the first factorial plan.
Bottom: Representation of the vectors related to the environmental parameters.
As we can see in figures 11 and 12 the second, third and fourth layers do no show any apparent
difference between the two sampling sites, and that is why they are grouped. For the first layer
the items related to Eucaliptal are circumscribed to a smaller area, although they are in the
same area than Hortas.
The first layers are grouped according to the two seasons. In Summer the second, third and
fourth layers are all grouped, while in Autumn they are individualised. The fourth layers do not
show differences between the two seasons.
The trends observed in this analysis are the following: two groups related to the first layer, one
the Summer (HS1 and ES1) and another for Autumn (HA1 and EA1); a group related to the
second layers in Autumn (HEA2), another group related to the third layers in Autumn (HEA3);
and a last group including the second and third layers in Summer (HES2 and HES3) and all the
fourth layers (HE4).
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Figure 12 – Identification of the different groups resulting from the correspondence analysis. The
arrows indicate the depth increase: the blue arrow in Summer and the black arrow
in Autumn.
The groups Rotifera, Turbellaria e Ciliophora and the crustacean nauplii are associated to the
first layers in Autumn. The Sarcomastigophora are associated to the first layers in Summer. The
Polychaeta occurred deeper, that is why they are associated to deeper layers. Although the
other groups also occurred in deeper layers they presented higher densities in the first layers
and that’s why they are closer to them.
The chlorophyll a and pheopigments concentration and the water and organic matter content
varied inversely to depth and presented higher values in Autumn what might have conditioned
the direction of the vectors that are pointing to the fist layers, mainly the Autumn ones. The
organic matter content increase from Summer to Autumn was not very significant, so the related
vector is in an intermediary position. The mud content is essentially associated to the Hortas
samples since in this place the values were always greater than 99%.
4.1.4
Discussion
Oxygen availability is one of the main factors that condition the vertical distribution of meiofauna
(Coull, 1988). According to Cartaxana & Lloyd (1999) the oxygen concentrations measured in
muddy sediment of the low salt marsh of the Tagus estuary reach very low values already in the
first millimetre. They continue to fall in the second millimetre and keep on falling, although not so
sharply until they became undetectable at 14mm depth. Bioturbation also brings oxygen to
anoxic zones (Fenchel, 1996; Forster, 1996). According to Forster (1996) the great spatial and
temporal heterogeneity of these oxidation states can affect the meiofauna migration and the
biogeochimical processes. Therefore and since the first layers are always muddy the sediment is
oxidised only very close to the surface; in the second layer if oxygen is still present its level will
be very low and it will disappear altogether in the third and forth layers.
Oxygen may also be present in anoxic zones due to the bioturbation already mentioned caused
by tube-dwelling animals.
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The oxygen availability limits the distribution of several meiobenthic groups that can be found
almost exclusively in the first layer (Copepoda, Rotifera, Turbellaria, Ostracoda, Bivalvia,
Gastropoda and nauplii).
Although the groups Nematoda, Sarcomastigophora, Polychaeta, Oligochaeta and Halacaroidea
often show higher densities in the first layer they also attain high values and sometimes higher in
lower layers. Apparently the groups Polychaeta, Oligochaeta and Halacaroidea don’t show any
vertical distribution pattern. Since they are active diggers they can live at depths greater than the
10cm used in this study; this can explain why it is not possible to find any vertical distribution
pattern.
In the Sarcomastigophora group the organisms are fixed. Therefore it may be difficult to
distinguish living organisms from those that were dead by the time they were caught although
they were also stained. For this reason the density values of this group may be overestimated
for the lower layer. According to Gooday (1988) the Sarcomastigophora group is generally found
near the sediment surface where they can find nutrients and interstitial water is well aerated.
Since these organisms feed on algae (Gooday, 1988) and the food availability is higher on the
sediment surface, as we can see by the chlorophyll a in figure 2, their distribution tends to
decrease as the depth increases although according to Moodley et al. (1998b) the foraminifers
(Sarcomastigophora) can migrate through anoxic zones what suggests that some of them are
facultative anaerobes. According to the same author (1998c) the sulphide concentration (often
correlated with the absence of oxygen) may be important to determine their distribution since
they tolerate sulphide but only for survival effects, as they do not reproduce in its presence.
The Nematoda group has shown two different vertical distribution patterns according to the
season. In Summer it occurred almost exclusively in the first layer, like the other groups, while in
Autumn their abundance in the second layer was also very high and sometimes even higher.
Although the Nematoda density has increased between Summer and Autumn, their density in
the first layer decreased and there was a vertical redistribution of the individuals which were also
found in the second layer. According to Montagna et al. (1983) in muddy sediments when the
temperature rises the depth of the redox potential discontinuity decreases, i. e. moves closer to
the surface. Thus due to the sun exposure and the high temperatures the sediment underwent in
Summer the RPD depth is lower and the tolerance limits for each organisms moved upwards and
influenced their vertical distribution. According to the same author, this effect also conditions the
diatom distribution what explains the same patterns seen as regards the chlorophyll a
concentration.
According to De Deckere et al. (in prep.) the Nematoda migrate during a tidal cycle and can
migrate into the sediment reaching 15mm deep. Thus in favourable conditions exist in deeper
layers the Nematoda could also have migrated into this layers.
As regards the groups Insecta, Isopoda and Tardigrada, the small number of individuals (2, 1
and 1 respectively) didn’t allow any conclusions to be taken as regards the vertical distribution
patterns.
According to Soetaert et al. (1995) Nematoda were the dominant group in the Tagus estuary
followed by Copepoda, while in this work the second dominant group for both places is
Sarcomastigophora in both places and in Autumn, the Turbellaria group in Hortas and Ciliophora
group in Eucaliptal, although the densities of other groups were also high.
As regards seasonality this is apparent in almost all meiobenthic groups, as well as the
chlorophyll a values. This shows that microphytobenthos increased between Summer and
Autumn too.
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As can be seen in figure 8 the greatest differences occurred between the two seasons but there
were also differences between the two sampling sites. These differences are more relevant in
the upper layers and all the first layers are well separated and those relating to Summer are
distinct from those relating to Autumn. As already seen the second and third layers relating to
Autumn are also separated due to the great number of Nematode present in them. The fourth
layers are separated neither by season nor by site. So the seasonality effect gradually
disappears, as the depth increases, i. e. it is evident in the first layer but it is not seen between 6
and 10cm.
This decreasing effect of seasonality can also be seen for the chlorophyll a values which in the
fourth layer are all equivalent to and in accordance with the values found by Brotas & Serôdio
(1995) for the same depth in the Tagus estuary.
As it has already been said, according to Montagna et al. (1983) in muddy sediments when
temperature rises the RPD depth decreases and animal densities also decrease. This appears to
be the factor responsible for the lower densities this author obtained in Summer. In the Tagus
estuary the exposed sediment is subjected to higher temperatures in Summer than in Autumn
and this has a bear on the RPD depth.
In Hortas, the water content is rather lower in Summer than in Autumn. This difference is only
seen in the upper layers what indicates that it has been evaporation, probably due to the higher
temperatures felt in Summer and which results in a greater evaporation of interstitial water. In
Eucaliptal, the granulometry of the sediment is rather different which difficult any comparisons as
regards the water content since this is basically conditioned by the granulometry of the sediment
(Calvário, 1982).
According to Coull (1985) in muddy sediments the seasonal abundance is negatively related to
salinity. In Summer due to sun exposure, high temperatures and water evaporation, the salinity
of interstitial water can reach high values which together with the high temperatures and the
lower RPD depth may be responsible for the lower density and diversity seen in Summer.
The chlorophyll a/pheopigments ratio increases between Summer and Autumn which complies
with the results of Brotas et al. (1995). The fact that more and better food was available, since
the number of living algae increase as compared with detritus, has also provided better
conditions for meiofauna growth as they mainly feeds on detritus, diatoms and bacteria (Coull,
1988).
From Summer to Autumn, the mean density of meiofauna per core increased in Hortas and also
in Eucaliptal, although not in such a clear way. This was probably due to the fact that in the
latter site the samples collected in Autumn were from sediments with a higher content of sand
what can change the meiofauna densities and implies lower densities of microphytobenthos
(Brotas et al., 1995; Brotas & Serôdio, 1995).
This increase from Summer to Autumn is also seen in the percentage of organic matter, what
again indicates that the food availability increased from Summer to Autumn.
Although spatial correlation has already been documented (e. g. between Copepoda abundance
and the microphytobenthos (Blanchard, 1990; Sandulli & Pinckney, 1999; Santos et al., 1995),
this work didn’t show that type of correlation, as it would be necessary to use a rather different
method especially aimed at that kind of study. In addition, according to Montagna et al. (1983)
the physical factors apparently influence meiofauna and diatoms in the same way. So a simple
correlation between the variation of chlorophyll a values and densities of meiobenthic groups
may not mean a response from Copepoda to the varying quantity of food.
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As Nematoda are the dominant group of the estuarine meiofauna the seasonality of meiofauna is
closely linked to the seasonality of this group and according to Li & Vincx (1993) the abundance
peaks of the Nematoda dominant species may occur in Spring, Summer, Autumn and Winter.
This work did not cover an annual cycle so it could not be determined when the abundance peak
of this group and all the meiobenthos in the Tagus estuary will occur.
According to Bouwman (1987) when there is seasonality, the density of estuarine meiofauna
increases generally in Spring after the low values seen in Winter. A second peak can occur in
Autumn although the abundance peak of each group may occur in other seasons of the year
(Coull, 1988). This is the case of the Sarcomastigophora group that as opposed to the trend
seen in other groups decreased its density between Summer and Autumn in Eucaliptal.
In most studies the abundance peak of meiofauna occurs at the end of Winter or in the beginning
of Spring (Coull, 1985; Vincx, 1989; Rutledge & Fleeger, 1993; Li et al., 1996; Santos et al.,
1996; Coull, 1999). In studies made in the Ems estuary the abundance peak is seen in Summer
(Bowman et al, 1984; Essink & Keidel, 1998). In the Mira estuary, a study developed by Adão &
Marques (1999) shows higher values for the Nematoda group at the end of the Winter.
Although there are exceptions, such as the work performed by Vincx (1989) during three years,
the work of Li & Vincx (1993) that lasted for seven years and the work of Coull (1985) that lasted
for eleven years and was extended for 22 years (Coull, 1999), great part of the studies that
include time variations are based in periods of about one year (e.g. Bell, 1979; Montagna et al,
1983; Bowman et al, 1984; Rutledge & Fleeger, 1993; Blome & Faubel, 1996; Santos et al.,
1996; Li et al., 1996; Essink & Keidel, 1998; Adão & Marques, 1999).
According to Coull (1985) the interannual variability is much greater than the seasonal variability
and so the comparison of seasonality patterns should be considered with some care.
In the study performed by Soetaert et al. (1995) the samples were collected in April 1992. The
values of the total abundance of meiofauna were rather lower than those found in this work. In
the former work the highest mean density was approximately 2000 ind / 10cm
2
and the lowest
approximately 400 ind / 10cm
2
, while in this work the mean values per core varied from 3587 to
6965 ind / 10cm
2
(fig. 6). Although in Soetaert et al. (1995) work the samples were collected
only until 5cm deep and in this work until 10 cm deep, the difference between the densities is
still high, since we found more than 90% of meiofauna in the first 6 cm deep (fig. 4).
As it has already been said, interannual variability is much greater than seasonal variability
(Coull, 1985); so it can not be said that in the Tagus estuary the densities are lower in Spring
than in Summer and Autumn, although in the work developed by Danovaro (1996) in the North of
Italy the highest abundance peak was seen in October and the lowest in April. A similar
seasonality pattern could exist in the Tagus estuary.
Since the sampling sites considered by Soetaert et al. (1995) show very different conditions of
granulometry and salinity, it is difficult to compare the density and diversity seen in the two
works. The four sampling sites are placed along a salinity gradient and the site that shows
salinity equivalent to the two sites studied in this work is sandy and it only has 36% of mud. As
the work performed by Soetaert et al. (1995) is mainly aimed at Nematoda it only shows density
values related to the groups Nematoda, Copepoda, Gastrotricha, Turbellaria, Ciliata e
Foraminifera. Therefore an overall comparison of the results of both studies is not possible.
4.2
Benthic Macrofauna
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4.2.1
Sampling sites
Sampling took place seasonally between Autumn 1998 and Summer 1999 in the two sites
established: Hortas, near Ribeira das Enguias, and Vasa Sacos, near the mouth of the Sorraia
River (Fig. 13).
Figure 13 – Representation of both sites sampled for the benthic macroinvertebrate
communities
At each site sampling stations were located in:
- mudflats which are flooded daily and have an altitude between -0,8 m and -0.1 m
(mean sea level).
- creeks mouth which is the transition area between the mudflats and the creek.
- creeks that are also flooded daily and have an altitude between –0.1 m and 0.2 m
(mean sea level).
- the pioneer area covered by Spartina maritima has a altitude, in relation to mean
sea level of 0.6, being daily flooded excepted during neap tides.
- the creek margins covered mainly by two species of salt marsh plants: Halimione
portulacoides and Arthrocnemon perenne. This area presents an altitude of 1.2 m (mean sea
level) being submersed during Spring tides.
4.2.2
Methodology
Sediment analysis
Sediment samples for determination of the water and total organic matter content and
granulometric analysis were collected using a Van Veen grab or a core.
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Water content was assessed by drying the samples at 60ºC for 24 hours while the total organic
matter was determined after destruction in a muffle furnace (2h at 450ºC).
For the determination of the grain size, the sediment samples were dried at 60ºC, weighted and
washed to remove the fine portion (<63 mm) and dried again at the same temperature. Sediment
was then sorted in a 7 sieve series (2 mm, 1 mm, 500 µm, 355 µm, 250 µm, 125 µm and
63 µm) and weighted according to grain size. The fine fraction was determined in relation to the
initial sample dry weight.
Benthic macroinvertebrates sampling
Two different methods of sampling were used to collect benthic macroinvertebrates. In the
creeks and mudflats a Van Veen grab (with an area of 0.05 m
2
) was used. At the salt marsh
sites a core (0.12 m diameter) was used to collect sediment samples. To prevent decomposition
buffered formalin stained with Bengal Rose was added to the samples.
At the laboratory, the sediment samples were washed in a sieve with 500 µm mesh size. The
benthic invertebrates were than identified to the lowest level possible, counted and weighted.
Data were analysed through the evaluation of species richness S (expressed as the total number
of taxa in each site), density D (expressed in number of individuals per m
2
) and biomass B
(expressed in g of dry weight per m
2
) which was performed according to Ruhmor (1990). Two
indices were also used: Shannon-Wiener’s diversity H’ (Shannon and Weaver, 1963) and
evenness J (Pielou, 1966).
4.2.3
Results
Sediment analysis
As expected, for both sites, the values of total organic matter were always superior in the
stations with vegetation, pioneer and creek margin areas. In most of the seasons there seems to
be a gradient of the percentage of organic matter from the mudflat, with lower values, to the
creeks (Fig. 14).
In opposition the percentage water was higher in the areas with shorter flooded periods. An
exception was observed for the pioneer area in Vasa sacos where a series of small ponds retain
the water for a longer period.
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Figure 14 - Variation of the water content and total organic matter percentages in Hortas and
Vasa sacos during the Autumn, Spring and Summer. (M - mudflat, Cm - creek
mouth, C - creek, Sp – pioneer area, HA - creek margins)
The granulometric analysis revealed a high resemblance between all the stations with the
predominance of fine grains, always superior to 97%.
Species composition
In the salt marsh area a total of 37 taxa of benthic invertebrate were identified (Tab. II), 31 in
Hortas and 30 in Vasa sacos with annual average densities of 2707.3 and 1519.1 ind/m
2
,
respectively. The most abundant taxon in these areas was the oligochaetes. The ostracodes
were mostly present in Hortas, being the main responsible for the higher density in this area.
Table III - Benthic macroinvertebrates community taxa with average ind/m
2
) in each site.
Taxa
Hortas
Vasa sacos
Phylum Protozoa
Class Sarcodina
Order Forameniferida
Forameniferida n.i.
1.0
Phylum Nematoda
Nematoda n.i.
22.1
11.8
Phylum Annelida
Class Polychaeta
Order Errantia
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Family Nereidae
Hediste diversicolor
17.3
4.8
Nereidae n.i.
0.3
0.4
Order Sedentaria
Family Spionidae
Pygospio elegans Claparède
0.7
1.8
Polydora sp.
2.5
0.1
Streblospio shrubsolii Buchanan
117.1
125.1
Spionidae n.i.
2.1
7.0
Family Cirratulidae
Cirratulidae n.i.
1.8
Family Capitelidae
Capitelidae n.i.
45.8
Polichaeta n.i.
9.2
0.3
Class Oligochaeta
Oligochaeta n.i.
972.5
835.1
Phylum Mollusca
Class Bivalvia
Order Eulamellibranchia
Family Scrobicularidae
Scrobicularia plana (Da Costa)
83.1
9.4
Abra tennuis (Montagu)
3.3
Class Gastropoda
Order Mesogastropoda
Family Hydrobiidae
Peringia ulvae (Pennant)
175.1
40.2
Order Basommetophora
Family Ellobiidae
Phytia myosotis (Draparnaud)
28.9
88.5
Phylum Arthropoda
Class Arachnidae
Order Araneae
Araneae n.i.
5.2
Order Acari
Acari n.i.
2.2
1.7
Taxa
Hortas
Vasa sacos
Class Ostracoda
Ostracoda n.i.
916.8
1.1
Class Crustacea
Order Isopoda
Family Gnathiidae
Paragnathia formica (Hesse)
125.0
82.6
Family Anthuridae
Cyathura carinata (Kröyer)
26.0
33.8
Family Sphaeromatidae
Sphaeroma monodi Bocquet, Hoestlandt & Levi
62.7
149.7
Order Amphipoda
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Family Talitridae
Orchestia gammarela (Pallas)
20.6
Family Gammaridae
Gammaridae n.i.
1.0
0.7
Family Corophiidae
Corophium sp.
2.2
1.7
Amphipoda n.i.
0.7
Class Insecta
Order Diptera
Family Limoniidae
Limoniidae n.i.
48.1
31.3
Family Dolichopodidae
Dolicopodidae n.i. (larvae)
31.9
35.4
Family Chironomidae
Chironomidae n.i. (larvae)
19.1
Family Ceratopogonidae
Ceratopogonidae n.i. (larvae)
0.7
Diptera n.i. (Pupae)
1.8
3.2
Order Coleoptera
Coleoptera n.i (larvae)
4.4
3.7
Order Homoptera
Homoptero n.i (larvae)
0.1
Insecta n.i. (larvae)
1.8
2.2
Insecta n.i. (adulto)
1.5
The most represented groups were the polychaetes, isopods and insects. Within the
polychaetes, Streblospio shrubsoli clearly dominated in both sites. In the case of isopods
diferent species dominated, Paragnathia formica in Hortas and Sphaeroma monodi in Vasa
sacos. The same happened with the insects, with Limoniidae and Dolichopodidae larvae being
the most abundant in Hortas and Vasa Sacos respectively. Although the two species of
gastropods were identified in both sites, Peringia ulvae revealed the highest density in Hortas
while in Vasa sacos it was Phytia myosotis .
The analysis of the macroinvertebrates taxa per site (Tab. IV) showed that in the mudflats,
creeks mouth and creeks habitats the communities were dominated by oligochaetes,
polychaetes (mainly S. shrubsolii) and ostracodes (only in Hortas), presenting higher densities in
the mudflats. The bivalve Scrobicularia plana and the gastropods P. ulvae were also abundant.
All these taxa presented lower densities in Vasa sacos. However, there were some differences
between the creeks habitat and the mudflats and creeks mouth habitats, not only on the
abundance of the taxa refered (specialy for Hortas), but also on the higher representativity of
insect larvae taxa which was much lower in these two last habitats.
In what concerns the biomass values, S. plana was the dominant taxa in the mudflats and in the
creeks mouth of both areas. P. ulvae and ostracodes in Hortas and Hediste diversicolor and
oligochaetes in Vasa sacos also presented high values of biomass in these habitats. Inside the
creeks the relative importance of the polychaete H. diversicolor and of the isopod Cyathura
carinata increased, while there was a decrease in the biomass values of S. plana, specialy in
Hortas.
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The pioneer vegetation areas showed, in Vasa sacos, the poorest benthic community, though
most of the taxa presented considerable densities, namely P. ulvae with 118.0 ind/m
2
. This
area, in both sites, was characterised by the increase in abundance of many taxa, especially
insects and isopods. In Hortas the oligochaetes clearly dominated, but with several other taxa
like P. formica, S. monodi and P. ulvae registering values above 200.0 ind/m
2
. Regarding the
biomass, the values observed in Vasa sacos were lower than those in Hortas but P. ulvae had
the highest values in both, 0.4 and 7.6 g/m
2
, respectively. S. plana registered a decrease in its
densities, nevertheless in Hortas it was still important in terms of the biomass.
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Table IV – Average density (ind/m
2
) and biomass (g/m
2
) of the important benthic
macroinvertebrate community taxa in both sites.
Taxa
Hortas
Vasa sacos
Mudflat Creek
mouth
Creek Pionee
r area
Creek
margin
Mudflat Creek
mouth
Creek
Pionee
r area
Creek
margin
D
B
D
B D
B D
B D
B
D
B
D
B D
B
D
B D
B
H.
diversico
lor
8.1 4.4
´10
-2
3.8 7.
9
´1
0
-2
4.3 6.
5
´1
0
-2
25.
8
0.
2
44.
2
0.9 7.4 9.2
´10
-2
11.
1
8.
6
´1
0
-2
5.6 4.5
´10
-
2
S.
shrubsoli
i
130
.0
4.6
´10
-3
300
.2
1.
1
´1
0
-2
132
.8
5.
4
´1
0
-3
22.
1
7.
4
´1
0
-4
189
.1
6.0
´10
-3
156
.9
7.
0
´1
0
-3
265
.0
1.6
10
-
2
14.
7
-
Spionida
e n.i.
9.8 -
0.7 7.
1
´1
0
-5
24.
0
-
3.7 -
7.4 -
Oligocha
eta n.i.
323
.6
1.0
´10
-2
335
.7
1.
3
´1
0
-2
230
.0
7.
3
´1
0
-3
187
6.8
5.
0
´1
0
-2
209
6.2
8.4
´10
-
2
195
0.2
7.6
´10
-2
649
.7
2.
2
´1
0
-2
118
0.9
7.4
´10
-
2
88.
5
1.
5
´1
0
-3
306
.0
6.
9
´1
0
-3
S. plana 216
.2
14.
0
185
.0
0.
3
3.1 1.
7
´1
0
-2
11.
1
7.
6
30.
6
14.
6
8.8 3.
0
7.5 0.4
P. ulvae 150
.9
0.5 238
.7
0.
4
30.
8
6.
8
´1
0
-2
317
.1
7.
7
138
.3
1.8 31.
9
9.2
´10
-2
12.
4
2.
3
´1
0
-2
38.
7
3.0
´10
-
2
118
.0
0.
4
P.
myostis
0.7 5.
0
´1
0
-4
11.
1
-
132
.7
1.2
´10
-
2
442
.5
1.
8
´1
0
-2
Ostracod
a n.i.
155
3.2
0.1 298
0.2
0.
2
50.
5
2.
5
´1
0
-3
1.8 -
3.7 -
P.
formica
320
.8
0.
1
304
.2
9.3
´10
-
2
413
.0
8.
3
´1
0
-3
C.
carinata
13.
8
5.8
´10
-3
3.8 1.
4
73.
7
2.
8
38.
7
7.7
´10
-
3
33.
7
2.4
´10
-2
11.
1
9.
4
21.
0
4.7
´10
-
2
73.
7
5.
8
29.
5
4.
1
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´1
0
-2
´1
0
-2
´1
0
-3
´1
0
-2
´1
0
-4
S.
monodi
221
.2
0.
1
92.
2
3.3
´10
-
2
1.3 1.6
´10
-3
2.5 8.0
´10
-
3
744
.8
7.
7
´1
0
-2
O.
gammar
ela
103
.2
2.
0
´1
0
-2
Corophiu
m sp.
11.
1
6.
6
´1
0
-3
1.3 1.9
´10
-
4
154
.9
2.
8
´1
0
-3
Limoniid
ae n.i.
2.9 3.
4
´1
0
-3
44.
2
1.
2
´1
0
-2
193
.6
6.4
´10
-
2
1.9 4.0
´10
-
3
70.
1
0.
4
Dolicopo
didae n.i
.
1.8
4
-
44.
4
1.
4
´1
0
-2
47.
9
5.
5
´1
0
-2
62.
7
1.2
´10
-
2
1.8 3.7
´10
-4
18.
8
6.
5
´1
0
-3
19.
9
9.4
´10
-
3
66.
4
8.
1
´1
0
-3
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In the creek margins, both sites presented similar benthic community structure, with a high
representativity of a large number of groups namely, isopods, amphipods, oligochaetes,
gastropods and insects. It was noticeable in these areas the reduced number of polychaetes, the
absence of bivalve species and the high number of insects taxa. The highest values of density in
the creek margins were registered for oligochaetes (2096.2 ind/m
2
) in Hortas and S. monodi
(744.8 ind/m
2
) in Vasa sacos. The gastropds, represented by P. ulvae and Phytia myosotis were
also abundant, and in Hortas P. ulvae had the highest value of biomass (1.8 g/m
2
) of this area
while in Vasa sacos, Dolicopodidae was the taxon with higher biomass value.
Seasonal Analysis
The analysis of the seasonal variation of the density and biomass in both sites showed that the
highest densities were obtain in different seasons, Winter for Vasa sacos and Summer for
Hortas. However these fact resulted from the high densities of ostracodes in the first site and of
oligochaets in the last one.
In terms of biomass the highest values were obtain during the Spring for both sites with 12.5 g/
m
2
and 17.5 g/m
2
respectively for Vasa sacos and Hortas.
In Hortas, the areas without salt marsh vegetation presented in the Autumn and Winter the
highest densities of oligochaetes while the ostracodes were mostly present during the Spring and
Summer.
Regarding the area colonised by S. maritima (pioneer area), P. ulvae was the most abundant
species in the Autumn (59.0 ind/m
2
) and Summer (1150.4 ind/m
2
) while during the Winter and
Spring it was substituted by S. shrubsolii (88.5 ind/m
2
) and oligochaetes (7477.9 ind/m
2
),
respectively. Nevertheless, in Autumn and Winter the number of taxa identified was very
reduced.
In the Spring, P. formica showed high densities in both areas where salt marsh vegetation was
present. In the area colonised by H. portucaloides and A. fruticosum (creek margin), only one
taxon was identified during Autumn and Winter. However an increase in the number of taxa was
observed in the Spring with the presence high densities of insect larvae (especially Limoniidae
with 774.3 ind/m
2
), isopods (mainly P. formica with 1216.8 ind/m
2
) and gastropods (P. ulvae,
376.1 ind/m
2
and P. myosotis , 531.0 ind/m
2
). During the Summer this area was clearly
dominated by oligochetes (3849.6 ind/m
2
) which corresponded to about 89% of the total number
of individuals captured.
In terms of biomass, in the Hortas mudflat it was S. plana the dominat species, except during the
Autumn (P. ulvae). It was also in this area that during the Spring the highest value of this
parameter, for all sampling areas, was registered (46.2 g/m
2
). In the creek mouth and creek area,
in most seasons, the same species dominated, P. ulvae during the Autumn and Summer and H.
diversicolor in the Winter. In the areas colonised by salt marsh plants it was P. ulvae that had
the highest biomass values in the Spring and Summer, though in the pioneer area during the
Spring, S. plana revealed the highest value (31.0 g/m
2
) of the two areas.
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In Vasa sacos the oligochaetes were the dominant group in almost every areas without
vegetation for most of the sampling period. However, during the Summer in the creek area the
most abundant taxon was P. ulvae with 120.0 ind/m
2
, while in creek mouth it was S. shrubsolii
(35.0 ind/m
2
)
In the pioneer area insects’ larvae and the gastropods were the most represented group during
the Summer. In the remaining seasons few taxa were present in the area.
In creek margins, during the Autumn and Winter only insects’ larvae were identified. This area
was dominated, in the Spring by P. formica and oligochaetes with densities of 1651.9 ind/m
2
and
1062.0 ind/m
2
, respectively. This last taxon, along with nematodes was, during the Summer, the
most abundant groups although their densities were inferior to those registered in Spring.
The areas without vegetation revealed that in most seasons where S. plana was present the
highest values of biomass belong to this species. However, duringt the Autumn in the mudflats
and in the Summer for the creek area, the oligochaetes and P. ulvae, respectively presented the
highest biomasses. When S. plana wasn’t captured, two taxa dominated, H. diversicolor in the
creek mouth ( Autumn and Winter) and C. carinata in the creek (Autumn). For the pioneer area it
was clear that P. ulvae was the most important species in terms of biomass. Only during the
Spring, when P. ulvae wasn’t identified, the isopod C. carinata had the highest biomass value. In
the creek margin different taxa presented the highest taxa. Thus, during the Autumn ans Winter
it was the Dolichopodidae larvae, while in the Spring and Summer, the species that most
contributed for the biomass were the isopod S. monodi and the gastropod P. myosotis ,
respectively.
Specific richness, diversity and evenness
The analysis of the specific richness, diversity and evenness for both sites during the Autumn,
Winter, Spring and Summer (Tab. V) showed that the diversities in Vasa sacos were in most of
the cases lower than in Hortas. This seemed to be related with the reduced values of evenness
in that site, originated by the higher dominance of one taxon, oligochaetes.
In general, in Hortas, the areas without vegetation were the ones with the highest values of
diversity, mainly due to the reduced number of taxa present in the areas with vegetation.
However in Spring, with the increase of the specific richness, the areas colonised by vegetation
registered high diversity values (1.083 in the pioneer area aand 1.556 in the creek margin).
For the creek and the mudflat the seasonal flutuations of all the parameters were very reduced.
In oposition the creek mouth presented a high seasonal variability in the diversity values mainly
due to the flutuation in the number of species captured.
In Vasa sacos the dominance of oligochaetes from Autumn till Spring was responsible in the
areas without vegetation, for the low values of evenness and diversity, between 0.186 and 0.408
in mudflats during the Autumn and 0.526 and 1.155 in the Spring for the creek. In Summer, due
to the reduction in the relative importance of the oligochaetes, and thus the increase of the
eveness values, the diversity reached higher values (1.292 in mudflats, 1.331 in creek mouth
and 1.513 in the creek). In the areas colonised by salt marsh plants it was observed a similar
pattern as described for Hortas, with a very reduced species richness during the Autumn and
Winter and an increase of this parameter during the Spring which originated high diversity
values.
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Table V - Specific richness (S), diversity (H’) e evenness (J) of the benthic macroinvertebrate
community in Hortas and Vasa sacos
Hortas
Vasa Sacos
Mudf
lat
Cree
k
mou
th
Cre
ek
Pione
er
area
Cree
k
marg
in
Mudfl
at
Cree
k
mou
th
Cre
ek
Pione
er
area
Cree
k
marg
in
Autu
mn
S
10
5
7
2
1
9
7
7
3
1
H
’
1.540
1.08
2
1.35
4
0.637
0.000 0.408
0.71
8
0.63
5
0.860
0.000
J
0.669
0.67
2
0.69
6
0.918
-
0.186
0.36
9
0.32
7
0.783
-
Winte
r
S
8
7
8
3
1
6
6
7
3
2
H
’
1.581
1.17
3
1.49
7
1.011
-
0.611
0.75
7
0.80
6
0.956
0.693
J
0.760
0.60
3
0.72
0
0.921
-
0.341
0.42
3
0.41
4
0.870
1.000
Sprin
g
S
7
1
8
12
13
7
5
9
2
16
H
’
1.552
0.00
0
1.35
9
1.083
1.556 0.820
0.73
0
1.15
5
0.693
1.945
J
0.797
-
0.63
6
0.436
0.606 0.421
0.45
4
0.52
6
1.000
0.702
Sum
mer
S
11
12
8
4
8
9
4
7
8
6
H
’
1.120
0.93
0
1.51
0
0.734
0.487 1.292
1.33
1
1.51
3
1.562
1.229
J
0.467
0.37
4
0.72
6
0.530
0.234 0.588
0.96
0
0.77
7
0.751
0.686
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4.3
Fish assemblages in tidal salt marsh creeks and in adjoining mudflat areas in the
Tagus estuary
4.3.1
Introduction
The importance of salt marshes as nursery habitats for fish has been emphasised by several
authors, mainly for eastern USA estuarine systems (e.g., Cain & Dean, 1976; Weinstein &
Brooks, 1985; Rozas 1995).
For European estuaries, some studies concerning the structure and dynamic of the fish
assemblages in salt marsh areas were also developed, namely those conducted by Labourg et
al. (1985), Drake & Arias (1991), Cattrijsse et al. (1994) and Costa et al. (1994). Despite these
contributions, knowledge on fish assemblages of European salt marshes is scarce.
Salt marsh tidal creek areas are characterised by a high instability due to fluctuations of water
level and the direction and strength of the flow, which induce a high variability in the abiotic
conditions (Labourg et al., 1985). Thus, the use of tidal creeks by fishes is controlled by the
hydroperiod. During high tide the creeks are flooded allowing the access of fishes. At low tide the
water drains almost completely being the fishes forced to move to the adjoining areas.
The utilisation of these habitats may be discussed in terms of cost-benefit. The high instability of
abiotic factors increases the risk of stranding and enables the occurrence of a large number of
species. Fish species that tolerate such conditions can benefit of the high food availability
induced by the extreme productivity of these marsh areas (Shenker and Dean 1979). This fact
associated with the low predation pressure within those habitats emphasises its potential as
feeding grounds and refuges for fish (Cain & Dean, 1976; Shenker & Dean, 1979; Bozeman &
Dean, 1980).
The fish assemblages in salt marsh areas reflect a seasonal pattern with pulses of transient
estuarine species, which regularly colonise these shallow and intertidal areas (Bozeman & Dean
1980; Rozas 1995).
The role of the Tagus estuary as nursery for fish, particularly the upper areas has been reported
in a large number of studies (e.g., Costa, 1982; Costa & Bruxelas, 1989; Cabral, 1998; Costa &
Cabral, 1999). According to these authors, the most important grounds are located in the
adjoining areas of salt marshes. The most abundant fish species that use these nursery grounds
are sea bass, Dicentrarchus labrax (L. 1758), and soles, Solea solea (L. 1758) and Solea
senegalensis Kaup 1858. However, no studies focused the role of the salt marsh areas for the
fish assemblage and the interaction between these habitats.
In the present paper a comparative analysis of the fish assemblages in two salt marsh tidal
creeks and their adjoining mudflat areas was performed in order to understand the relative
importance of these habitats for the Tagus fish community.
4.3.2
Methodology
Study Area
The Tagus estuary has an area of 320 km
2
, of which 113,8 km
2
are intertidal. About 13 km
2
of
the intertidal area is covered by salt marsh vegetation (Catarino et al., 1985). The Tagus estuary
is mesotidal with semi-diurnal tides and a tidal range of about 4 m.
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The present study was carried out on two salt marsh areas located in the upper part of the
estuary (Fig. 15). This region is characterised by an extensive area of mudflats composed of fine
muddy sediments, with 90,6% of particles with less than 20 mm diameter (Brotas et al., 1995).
On the upper part of the mudflats the pioneer/lower marsh areas are dominated by Spartina
maritima L. while the middle marsh is mainly composed by Halimione portulacoides L. and
Arthrocnemon perenne Miller, especially along the creeks.
Samples were taken in two tidal creeks (Hortas and Vasa sacos) and in the adjacent mudflat
areas (Fig. 15). The creek beds are approximately 150 m long, 15 m wide at the mouth and the
height between the mud bottom and the marsh surface is ca. 1.5 m.
Both creeks have no connection with other neighbouring creeks, drying almost completely during
ebb tides.
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Figure 15 - Location of the Tagus estuary and sampling areas.
Sampling methods
Two different sampling methods were used according to habitat. In the creeks, samples were
taken monthly from September 1998 until August 1999, during daylight at ebb tides of similar
amplitudes, using fyke and gill nets (3mm and 50mm mesh size, respectively). The gill nets were
used to capture the large specimens, mainly mugilids, and therefore to avoid the clog of the fyke
net.
Fishes were collected on each 30 min, from high tide until the creek was completely dry. At
each collection temperature and salinity were measured using a Hidrolab multiprobe sonde.
In the mudflat areas, samples were done monthly from January 1995 until December 1996 using
a 4 m beam trawl with 10 mm mesh size and one tickher chain. Trawls were towed at about 1
knot of speed and lasted 20 min. Three trawls were performed monthly per sampling area.
Temperature and salinity were also measured at each sampling period and area.
All fish caught were counted, measured (total length to the nearest 1 mm) and weighed (wet
weight with 0.001 g precision) in the laboratory.
Data analysis
Spearman rank correlation coefficient was calculated to compare the species abundance in the
creeks and in the mudflats (Zar, 1996).
The analysis of the structure of the fish assemblages was based on ecological and trophic guilds
(adapted from Elliott & Dewailly, 1995), indicating the species’ use of the estuary and the feeding
habits, respectively. Five ecological guilds (i.e. fresh water adventitious, marine adventitious,
catadromous, nursery and resident species) and four trophic guilds (i.e. detritivorous, strictly
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planktivorous, strictly invertebrate feeder and carnivorous other than the two previous guilds)
were used. The Chi-square statistic was used to test differences in the number of species per
guild (Zar, 1996).
For the most abundant species the percent of juveniles and adults individuals was determined
based on length at maturity reported by Almeida (1996) for Liza Ramada (Risso, 1826), Pestana
(1989) for Sardina pilchardus (Walbaum, 1792), Dinis (1986) for S. senegalensis, and
Bouchereau et al. (1990) and (1993) respectively for Pomatoschistus minutus (Pallas, 1770) and
Pomatoschistus microps (Krøyer, 1838).
Species richness (S), evenness (J) and Shannon-Wiener’s (H’) diversity indices were calculated
for each sampling area and season (Ludwig & Reynolds 1988).
4.3.3
Results
Abiotic conditions
The variation of the temperature values was similar in the two creeks as well as in the two
mudflat areas (Fig. 16). In both habitats, the maximum values were obtained in July and August
(23.3ºC and 22.5ºC in Hortas and Vasa sacos creeks, and 23.2ºC and 24.8ºC in the respective
mudflat areas). The minimum values were recorded in January and were lower in the creeks
(7.8ºC and 9.5ºC) comparatively to both mudflat areas (12.0ºC).
Figure 16 - Water temperature and salinity in the study areas during the sample period.
The maximum and minimum salinity values were obtained in the same months as the extreme
temperature values. The seasonal variation pattern was similar in all the areas (Fig. 16).
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Community structure
A total of 28 fish species were identified, of which 12 occurred in the salt marsh tidal creeks and
26 in the mudflat areas (Table VI). Species composition in the two intertidal creeks was similar
as well as in the two mudflat areas considered.
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Table VI - Relative abundance, biomass and ecological (FW- fresh water adventitious, MA-
marine adventitious, C- catadromous, N- nursery and R- resident) and trophic guilds
(D- detritivorous, P- strictly planktivorous, IF- strictly invertebrate feeder and C-
carnivorous other than the two previous guilds) of the fish species captured in the
salt marsh creeks and in the mudflat areas at Hortas and Vasa sacos.
Hortas
Vasa sacos
Creek
Mudflat
Creek
Mudflat
Species
EG TG
Nº
ind.
(%)
Biomas
s
(% g)
Nº
ind.
(%)
Biomas
s
(% g)
Nº
ind.
(%)
Biomas
s (% g)
Nº
ind.
(%)
Biomas
s
(% g)
Anguilla
anguilla
C
C
0.4
< 0.1
0.1
1.5
0.1
< 0.1
0.4
2.3
Atherina
presbyter
R
P
0.1
< 0.1
<
0.1
< 0.1
< 0.1 < 0.1
<
0.1
< 0.1
Barbus
bocagei
F
W
IF
<
0.1
1.1
Chelon
labrosus
N
D
<
0.1
0.7
0.1
3.6
Ciliata mustela N
C
<
0.1
0.1
<
0.1
0.1
Conger conger N
C
<
0.1
0.1
<
0.1
0.1
Dicentrarchus
labrax
N
C
0.3
< 0.1
7.7
4.8
< 0.1 < 0.1
1.0
0.9
Diplodus
bellottii
N
IF
0.1
< 0.1
Diplodus
sargus
N
IF
< 0.1 < 0.1
0.1
0.2
Diplodus
vulgaris
N
IF
<
0.1
< 0.1
Engraulis
encrasicolus
R
P
0.1
< 0.1
0.8
0.6
< 0.1 < 0.1
2.0
0.8
Gambusia
holbrookii
F
W
P
0.1
< 0.1
< 0.1 < 0.1
Gobius niger
R
IF
0.1
0.1
0.6
0.3
Halobatrachus
didactylus
R
C
<
0.1
< 0.1
Hippocampus
hippocampus
R
P
<
0.1
< 0.1
<
0.1
< 0.1
Liza aurata
N
D
0.1
< 0.1
0.1
0.3
0.1
1.0
0.1
0.2
Liza ramada
C
D
49.9
99.6
6.0
55.3
5.6
90.5
4.9
56.6
Mugil
cephalus
N
D
< 0.1 0.2
0.1
0.7
0.4
12.9
Platichthys
flesus
N
IF
0.3
2.2
0.1
0.5
Pomatoschistu
s minutus
R
IF
9.8
1.1
24.1 2.6
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Pomatoschistu
s microps
R
IF
46.4
0.1
58.
7
3.0
49.8
6.0
57.6 2.2
Raja clavata
MA C
<
0.1
< 0.1
<
0.1
0.5
Sardina
pilchardus
N
P
1.5
< 0.1
<
0.1
< 0.1
43.8
2.3
0.1
< 0.1
Solea
senegalensis
N
IF
15.
0
29.0
5.5
13.4
Solea solea
N
IF
0.1
0.2
0.5
1.2
Sparus aurata
N
IF
0.1
0.1
<
0.1
0.2
Syngnathus
thyple
R
P
<
0.1
< 0.1
Syngnathus
sp.
R
P
1.0
< 0.1
1.0
0.1
0.4
< 0.1
2.2
0.1
Total
2470
8
1052999 135
72
143873
4638
4
81261
707
9
95503
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The creeks fish assemblage was mainly composed by estuarine resident species and by marine
species that use the estuary as nursery (Fig. 17). Fresh water species were only present in
periods of intense rainfall, while marine occasional species were completely absent from these
areas. In the mudflat areas the number of species per ecological guild did not differ statistically
from creeks (C
2
= 1.664; d.f.= 4; p> 0.05). In that habitat the species that uses the area as
nursery was the most representative one, comprising 54% of the species in Vasa sacos and
50% in Hortas.
Figure 17 - Distribution of the fish species per ecological guilds (FW- fresh water adventitious,
MA- marine adventitious, C- catadromous, N- nursery and R- resident species) for
the saltmarsh creeks and for the mudflats at Hortas and Vasa sacos.
Considering the trophic guilds, no statistical differences were found between the creek and the
mudflat areas (C
2
= 2.876; d.f.= 4; p> 0.05). The planktivorous species was the predominant
group in the creeks (Fig. 18), especially in Vasa sacos where it was composed by 50% of the
species. Some carnivorous species were also present in these habitats. The detritivorous were
the only big-size species present in the creeks. In the mudflat areas, where the proportion of
species according to ecological guilds was more equable, the invertebrate feeders were the
predominant group, representing 32% in Hortas and 42% in Vasa sacos.
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Figure 18 – Distribution of the fish species per trophic guilds (D- detritivorous, P- strictly
planktivorous, IF- strictly invertebrate feeder and C- carnivorous other than the two
previous guilds) for the saltmarsh creeks and for the mudflats at Hortas and Vasa sacos.
No statistical differences were found in the species abundance between both creeks(r=0.937;
p<0.05) and mudflats (r=0.815; p<0.05). However, the abundance in the creeks was significantly
different from the mudflats (r=0.345; p>0.05).
Three species were numerically dominant in the creeks, comprising over 95% of the total
number of individuals captured: S. pilchardus (43.8% in Vasa sacos), L. ramada (mainly in
Hortas with 49.9%) and P. microps in both creeks (46.4% and 49.8% respectively for Hortas
and Vasa sacos). This species was also the most abundant in both mudflat areas, representing
more than 50% of the captures.
Although absent in the creeks S. senegalensis, in particular at Hortas (15.0%), and P. minutus,
mainly in Vasa sacos (24.1%), were also abundant in the mudflats.
In terms of biomass L. ramada was the most important species in all studied areas. The values
obtained for this species ranged from 91% to almost 100% in the creeks and from 55% to 57%
in the mudflat areas. In these zones S. senegalensis was also an important fraction of the
biomass, especially in Hortas where it represented 29.0% of the captures. In the creeks, the
total biomass observed for Hortas was more than 10 times higher than the value obtained for
Vasa sacos.
Seasonal variation
The diversity index (H’) for the creeks was always lower than in the mudflats and does not follow
the same pattern for both areas (Table VII). In Hortas the higher values occurred during the
Autumn when the specific richness (S) was higher and there were no dominant species. During
Summer the diversity values were very reduced following the same tendency of the evenness (J)
. In Vasa sacos the lowest values were observed during Winter when evenness was very
reduced. The highest diversity was obtained in Spring and Summer as a result of the increase in
the species richness and evenness index
Table VII - Seasonal values of species richness (S), evenness (J) and Shannon-Wiener’s (H’)
diversity indices for the salt marsh creeks and for the mudflat areas at Hortas and
Vasa sacos.
Hortas
Vasa sacos
Creek
Mudflat
Creek
Mudflat
H’
S
J
H’
S
J
H’
S
J
H’
S
J
Autumn
0.91
11
0.38
1.00
19
0.34
0.43
6
0.24
1.17
20
0.39
Winter
0.65
5
0.40
1.02
13
0.40
0.08
5
0.05
1.09
12
0.43
Spring
0.76
7
0.39
1.46
14
0.55
0.91
9
0.41
1.75
19
0.60
Summer
0.03
7
0.02
1.59
16
0.57
0.87
5
0.54
1.26
20
0.42
Both mudflat areas presented a similar pattern with highest diversities during Spring and
Summer following the increase of the evenness values.
The species present in the creeks showed a high seasonality (Table VIII) in the use of these
habitats. Only two species were captured during all the year, P. microps and L. ramada. A great
number of the species (e.g. Engraulis encrasicolus (L. 1758), D. labrax, Anguilla anguilla (L.
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1758), S. pilchardus and Liza aurata (Risso 1810)) were only captured during part of the year as
juveniles. The highest abundances for most of the species was observed during the Spring, while
in the Winter only a few individuals were caught, mostly from resident species.
The highest abundance of P. microps in the creeks was observed during Spring, mainly in Vasa
sacos, with a population composed mostly by juveniles. In the Summer there was a decrease in
the abundance of this species and the presence of adults in these areas was scarce. During the
Autumn/Winter the number of individuals increased again, although in this time mainly adults
were present. In the mudflat areas the highest number of individuals of this species was
observed during these late seasons followed by a gradual reduction of the abundances until the
Summer, when the concentration of individuals start increasing again.
L. ramada was always present in the creeks with a high number of individuals. Nevertheless, the
abundances in Hortas were always higher than in Vasa sacos. The exception was during Spring
when similar quantitatives, mostly small juveniles, were observed for both creeks. In the Summer
in Hortas, there was an increase in the number of captures of both juveniles and adults. In the
Autumn and Winter there was a gradual decrease of the abundance and mostly adults were
present in these areas. For both adjacent areas the peak of abundance of this species was
observed during the Winter. As described for the creeks, the number of individuals in Hortas was
always superior to that obtained for Vasa sacos.
In the creeks S. pilchardus was present, mostly in Vasa sacos, from the beginning of the Spring
until early Autumn. The highest abundance of this species was observed during the Spring when
small juveniles began to appear in these areas. In the Summer a marked decrease in the
number of individuals was observed leading almost to the disappearance of the species from
these areas. The presence of this species in the adjoining areas was very reduced.
In the mudflat areas P. microps was the most abundant species in most of the seasons with a
maximum during Autumn. Exceptions to this dominance were observed for Hortas in the Spring
when a high number of individuals of S. senegalensis and D. labrax were captured.
Table VIII - Number of individuals and percentage of juveniles per season for the most abundant
species captured in the salt marsh creeks and in the mudflat areas at Hortas and
Vasa sacos (Aut. – Autumn, Win. – Winter, Spr. - Spring, Sum. – Summer).
Hortas
Vasa sacos
Creek
Mudflat
Creek
Mudflat
Species
Aut. Wi
n.
Spr. Su
m.
Aut. Win
.
Spr. Su
m.
Aut
.
Win
.
Spr. Su
m.
Aut. Win
.
Spr. Su
m.
Dicentrarc
hus
labrax
80
100
%
5
100
%
14
100
%
1
100
%
748
100
%
278
100
%
6
100
%
3
100
%
40
100
%
26
100
%
Liza
ramada
125
4
45%
208
38
%
229
1
83%
856
5
87%
67
98%
594
67%
119
53%
32
81%
29
71
%
11
81
%
234
3
99%
217
35%
74
71%
155
25%
99
46%
16
50%
Pomatosch
istus
minutus
406
0%
735
2%
26
6%
168
408
1%
185
0%
191
12%
924
18%
Pomatosch
istus
microps
170
7
40%
71
2%
956
9
98%
17
57%
422
2
6%
274
9
1%
312
6%
687
1%
301
11
%
172
4
6%
204
92
95%
603
88%
168
8
0%
760
0%
429
5%
119
9
5%
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Sardina
pilchardus
4
100
%
368
100
%
5
100
%
2
100
%
203
07
100
%
20
100
%
2
100
%
1
100
%
1
100
%
2
100
%
Solea
senegalen
sis
666
100
%
99
100
%
770
100
%
497
100
%
128
100
%
44
100
%
91
100
%
129
100
%
4.3.4
Discussion
The different sampling methodologies used for salt marsh creeks and adjoining mudflats areas
enabled a direct comparison between both habitats. Unlike the fyke, that is almost a unselective
gear, the beam-trawl underestimates the abundance of both large and fast swimming specimens,
namely mugilids, and small fishes (considering the differences in mesh size comparatively to the
fyke net used). However the same sampling technique could not be applied in both habitats due
to their different characteristics. These constraints were considered for the selection of the
analytical tools to compare the fish assemblages of these two habitats.
From the 48 species reported in recent studies conducted in the Tagus estuary (Costa et al.
1998; Cabral 1998) only 26 were present in salt marsh mudflat areas and 12 in intertidal creeks.
The low number of species in the creeks suggested that only a limited number of the fish
species that occurred in the upper part of the estuary used those habitats. The fish species
richness in intertidal creeks reported for other European estuarine systems varied. In the North
Sea, Cattrijsse et al. (1994) reported the occurrence of 13 fish species in the salt marsh creeks
of the Westerschelde estuary while Laffaille et al. (1998) found 23 fish species in the creeks of
the macrotidal system of Mont Saint-Michel. Higher species richness (39 species) was obtained
for the Cadiz Bay (Drake & Arias, 1991). However, these creeks were subjected to a high marine
influence, which surely induce an increase of fish species number.
The number of fish species reported in studies conducted in USA estuarine salt marsh areas
also differed substantially (e.g., Shenker & Dean, 1979; Weinstein et al., 1980; Yoklavich et al.,
1991). As pointed out by Cattrijsse et al. (1994) these differences may be due to latitudinal
effects, but the particularities of both estuarine fish assemblage and salt marsh abiotic and biotic
conditions should be the major determinant of species richness.
Regarding the use of the estuary by the different species, the dominance of estuarine resident
species and fish that use the estuary as nursery noticed for the creeks assemblages in the
Tagus, was also outlined for other estuaries (e.g., Rozas, 1995; Kneib, 1997).
In terms of feeding habits, the dominant trophic group in two habitats was different. The
comparison of the food availability in these two areas would be extremely useful to explain the
preponderance of planktonic feeders in the creeks and of benthic feeders in the mudflat areas.
The low abundance of piscivorous species was a common aspect of the creeks fish
assemblages, reported by several authors (e.g., Cain & Dean, 1976; Miltner et al., 1995).
A general characteristic of tidal creeks fish assemblage is the dominance, both in number and
biomass, by few species (Cain & Dean, 1976; Kneib, 1984; Rakocinski et al. 1992; Cattrijsse et
al., 1994). In several studies conducted in European estuaries, P. microps (Drake and Arias
1991; Catrijsse et al. 1994) and L. ramada (Drake & Arias, 1991; Laffaille et al., 1998) has been
pointed out as the most important fish species in tidal creeks, as observed in the present study.
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Laffaille et al., (1998) in Mont Saint-Michel noticed a low abundance of P. microps but other
Gobiidae, P. minutus and P. lozanoi (de Buen, 1923), presented high densities in tidal creeks. In
the Tagus and also in other estuaries (Drake & Arias, 1991; Catrijsse et al. 1994) P. minutus
was abundant in the salt marshes adjoining areas but not in tidal creeks. These findings suggest
that, depending of site characteristics, a spatial segregation may be observed in alternative
estuarine habitats such as salt marsh creeks.
Drake & Arias, (1991), Catrijsse et al., (1994) and Laffaille et al., (1998) found also other fish
species, namely Platichthys flesus (L. 1758), S. solea, S. senegalensis and D. labrax in tidal
creeks. In the Tagus, some of these species were particularly abundant in the adjoining areas,
but were only occasionally caught in the creeks. Since the use of tidal creeks can be view under
a cost-benefit perspective, a comparative analysis of the food availability in these two estuarine
habitats could help explaining the absence of these species in tidal creeks.
Despite the similarities in variation pattern of temperature and salinity recorded in the two creeks
analysed in the present study, several differences in species abundance were found in the two
sites. Rakocinski et al., (1992) suggested that geomorphological characteristics of sites are
probably the most important factors determining habitat selection by fishes in estuarine tidal
creeks. The extension of the nearby mudflat area and the proximity to permanent subtidal areas
could support the differences in the abundance of L. ramada obtained between the two creeks
analysed.
Seasonal changes in the fish assemblages of tidal creeks, reflected mainly the recruitment or
pulses of abundance of different species. Some recruits migrate from other estuarine areas,
namely P. microps (Bouchereau et al., 1993), or from nearshore areas, namely L. ramada
(Almeida, 1996) and S. pilchardus (Ré, 1984).
The results obtained for the Tagus showed that diversity and evenness decreased in periods of
intensive recruitment, being the variation pattern different according to the site. Drake & Arias
(1991) outlined that these indices were higher in Winter and late Summer and both were
significantly correlated with density of resident species.
Most of the species described as using the upper Tagus estuary as nursery areas were absent
from the creeks or were occasional. Nevertheless, those areas are apparently important for P.
microps and L. ramada both as nursery areas and as feeding grounds for the adults. For S.
pilchardus the importance seems reduced comparing with the high densities of larvae observed
by Ré (1984) on the mouth of the estuary and on the adjacent coastal areas. However, the
analysis of the importance of these habitats for the fish community should include the role of the
different species as a trophic link between the highly productive salt marsh areas and the
adjacent estuarine areas or the nearby coastal areas. Laffaille et al. (1998) estimated that in
Mont Saint-Michel the fish community was responsible for the export of 50 tons DW of organic
matter per year, with the mullets responsible for 70% of this transport. The extremely high
biomass values of L. ramada in the Tagus tidal creeks associated with the foraging behaviour of
this species suggest the transport of a large amount of organic matter from the tidal creeks
towards adjoining estuarine areas or the nearby coastal areas.
5
TROPHIC ANALYSIS
For the study of the food web in the Tagus salt marsh two approaches were used:
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- multiple stable isotope analysis (C
13
/ C
12
, S
34
/ S
32
, N
15
/ N
14
) were applied to k-
species, representative of the different trophic levels, sellected after the biological
characterisation of the area;
- gut content analysis of the most representative fish species present in the study salt
marsh, the common gobie Pomatoschistus microps and the thin-lipped grey mullet Liza ramada.
Both methods were used in order to complement and compare between themselves.
5.1
Food habits of Pomatoschistus microps (Krøyer, 1838) in the Tagus salt marsh
5.1.1
Introduction
The common goby Pomatoschistus microps (Krøyer, 1838), is very common in estuaries,
lagoons and along the shores of Europe. In the Tagus estuary, studies of these species are
resumed to Costa (1988), Moreira (1991) and to Salgado (1995), this is possibly due to their low
economic value, despite their great abundance and extremely important role in the estuarine
food web (Costa, 1988). Their role in the diet of different organisms from Tagus estuary has
been emphasised by several authors, namely decapods, Crangon crangon Linnaeus and
Carcinus maenas Linnaeus, in teleosts like Anguilla anguilla Linnaeus (Costa et al., 1992), Solea
senegalensis Kaup and Dicentrarchus labrax Linnaeus (Cabral, 1998) and in piscivorous birds
such as Egretta garzetta Linnaeus (Moreira, 1992), Recurvirosta avosetta Linnaeus and Calidris
alpina (Moreira, pers. comun.).
The aim of this work is to deepen knowledge about the trophic place of P. microps in this salt
marsh food web and to understand seasonal changes in the feeding strategies of this species.
5.1.2
Methodology
This study was carried in two salt marsh tidal creeks located in the upper zone of the Tagus
estuary. These areas are described in detail in the analysis of the fish community section.
Field samples were taken monthly from September 1998 until August 1999, during daylight at
ebb tides of similar amplitudes, using fyke nets (3mm mesh size). Fishes were collected on each
30 min, from high tide until the creek was completely dry. At each collection temperature and
salinity were measured using a Hidrolab multiprobe sonde. After capture, gobies were placed on
ice to prevent post mortem digestion.
In the laboratory total length was measured to the nearest 1mm and wet weight was determined
to the nearest 0.0001g. For each species, a maximum of 60 digestive tracts, randomly selected,
were analysed every month per site. The food items found in the gastro-intestinal tracts were
identified to species whenever possible, counted and wet weighed to the nearest 0.0001g.
For quantitative analysis of the diet, occurrence (O
i
), numeric (N
i
) and weight (W
i
) frequencies
were used (empty digestive tracts were eliminated) as well as the dietary coefficient (Q
i
) a mixed
method proposed by Hureau (1970):
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Q
i
= N
I
x W
i
This method describes preferential (Q >200), secondary (200> Q >20) and accidental (Q < 20)
prey.
In order to know the variation of the feeding habits with the length, the individuals were grouped
into eight size classes of total length. Class I £ 19mm; 20mm £ class II £ 24mm; 25mm £ class
III £ 29mm; 30mm £ class IV £ 34mm; 35mm £ class V £ 39mm; 40mm £ class VI £ 44mm;
45mm £ class VII £ 49mm; class VIII ³ 50mm.
With the purpose of comparing the food ingested before and after the period of residence inside
the creeks, samples were performed during the flood on the mouth of the creek. The gut content
of the individuals sampled was analysed and the results were compared with the ones obtained
for the fish captured during ebb tide.
5.1.3
Results
The gut contents of a total of 442 Pomatoschistus microps, ranging from 10 to 51mm, were
analysed.
The polychaetes were the most frequent item in the diet of this goby (Table IX), occurring in 50%
of the gut contents analysed. However other items such as mysids (35.29%), bivalves (33.94%),
oligochaetes (28.96%) and isopods (27.60%) were also frequent.
Table IX - Occurrence (O), numerical (N) and weight (W) frequencies and dietary coefficient (Q
i
)
of the preys present in the gut contents of P. microps.
Taxa
%O
%N
%W
Q
i
Bivalves
33.94
11.30
41.30
466.76
Oligochaetes
28.96
27.38
7.33
200.69
Polychaetes
50.00
32.50
14.57
473.53
Isopods
27.60
7.86
3.88
30.53
Amphipods
9.50
0.80
4.23
3.39
Mysids
35.29
8.73
18.10
158.00
Copepods
10.41
7.52
0.02
0.16
Decapods
6.11
0.54
2.18
1.19
Insects
2.49
0.30
0.07
0.02
Fish
6.56
0.78
8.30
6.43
Others
4.30
2.28
0.02
0.04
According to the results of the dietary coefficient (Table I) three preys constitute the preferential
items in the feeding habits of P. microps. Polychaetes, mostly the spionidae Streblospio
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shrubsolii, bivalves, almost exclusively siphons of Scrobicularia plana, and Oligochaetes, with a
dietary coefficient of 473.53, 466.76 and 200.69, respectively. These results were mainly due to
the high weight component (41.30%) in the case of the bivalves, while for the annelids there was
a higher numerical contribution (32.50% and 27.38%, respectively for polychaetes and
oligochaetes).
Secondary preys were mysids with a high weight component (8.73%) and isopods, mostly
Sphaeroma serratum, with similar contributions from the numerical and weight components.
The seasonal analysis of the prey consumed by the common gobie (Table X) shows that the
polychaetes were preyed with abundance during the all year, representing always between 25
and 37% of the total preys ingested. However there were some fluctuations in the consumption
of other feeding groups.
The importance of the bivalves was mostly observed during the Autumn and Winter, respectively
with 17.07% and 14.44% decreasing in the other two seasons.
Table X - Numerical frequencies per season of the preys present in the gut contents of P.
microps.
Taxa
Autumn
Winter
Spring
Summer
Bivalves
17.07
14.43
7.69
5.21
Oligochaetes
13.46
47.39
20.07
13.96
Polychaetes
31.17
25.93
37.37
35.63
Isopods
8.81
9.81
6.59
4.38
Amphipods
0.48
0.46
1.20
0.63
Mysids
21.55
1.01
6.99
25.42
Copepods
1.12
0.59
16.13
0.21
Decapods
0
0
1.17
0.42
Insects
0.16
0.08
0.55
0
Fish
0
0.04
1.72
0
Others
6.17
0.25
0.52
14.17
In the Winter it was observed the higher consumption of oligochaetes, representing in this
season 47.39% of the total number of preys, although there was a marked decrease in the
abundance of this taxa during the other seasons, their numerical frequency was always superior
to 13%.
The ingestion of mysids was higher during the Summer and Autumn, while the copepods were
only important during the Spring with 16.13%, when the young of the year began to colonise
these areas.
The relative importance of the group “others”, which joins the remaining taxa, in the Summer is
due to the abundant presence of ostracods and acaridae during this season.
The analysis of the feeding habits of P. microps per length classes (Figure 19) shows that the
copepods were the most abundant taxa consumed by the individuals of the classes I and II,
representing in the class I (Lt £ 19mm) 78.70% of the total number of preys ingested.
Nevertheless, the mysids were also important part of the diet of this size individuals, as in for the
remaining classes. During the goby growth the importance of the copepods decreases, while the
polychaetes began to increase. Thus, in the classes III and IV this taxon was the most
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represented one with numerical frequencies superior to 30%, followed in order of abundance by
the mysids with near 19%.
Figure 19 - Numerical frequencies of the taxa ingested by de different length classes of P.
microps. Class I £ 19mm; 20mm £ class II £ 24mm; 25mm £ class III £ 29mm; 30mm £ class
IV £ 34mm; 35mm £ class V £ 39mm; 40mm £ class VI £ 44mm; 45mm £ class VII £ 49mm;
class VIII ³ 50mm.
For the length classes V, VI and VII the oligochaetes and the polychaetes represents more than
60% of the taxa consumed. However an increase in the abundance of bivalve siphons was
noticed. In the individuals with total length superior to 49mm (class VIII) the bivalves were the
most important item in numerical frequency with 33.68% followed in decreasing abundance by
oligochaetes and polychaetes. In this size class it was noted a higher abundance in the
consumption of a larger number of taxa.
From the total number of guts analysed during the ebb tides only 8.89% were empty.
The analysis of the gut contents of the 46 gobies collected during flood tides showed that 69.6%
were empty. Only 4 taxa were present on the remaining ones, fish (1 clean vertebral column),
spionidae (2 individuals), copepods (18 individuals) and gnathiidae (18 individuals).
5.1.4
Discussion
The diet P. microps included bivalves, gastropods, annelids, crustaceans, insects and fishes.
Such versatility was associated with their capacity to use different feeding strategies such as
biting and suction (Hamerlynck & Cattrijsse, 1994).
The preferential preys of the common goby were polychaetes, bivalves (siphons) and
oligochaetes. These preference for endobenthic preys were observed by other authors,
distinguishing polychaetes (Salgado et al., unpublished), the isopod Corophium volutator
(Magnhagen, 1986; Pihl, 1985) and bivalve siphons (Gee, 1985) as dominant preys.
Polychaetes, despite being present in the results obtain by these authors, never revealed the
importance assumed in the studies performed in the Tagus estuary.
Comparing with the results obtained by Salgado et al. (unpublished) for the upper estuary
subtidal areas, in the present study there was a higher abundance of epibenthic and pelagic
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taxa, as mysids, shrimps and fishes, while the presence of amphipods (mainly the benthic
Corophium volutator) and copepods (essentially harpacticoids) was higher and there were no
decapods in the guts analysed in that study. These difference in the results could be associated
with different prey availability in both sites and with the absence of P. minutus in the salt marsh
areas, a potential competitor for the same trophic niche.
This species is considered an opportunistic carnivore feeding on organisms that they select on
the basis of relative availability (Pihl, 1985). This fact is corroborated by the abundance of the
different preys on the digestive tracks of P. microps following their abundance in the creeks and
by the presence of a great number of juveniles of different species for which the presence in the
area is only seasonal.
Polychaetes and oligochaetes were the only taxon abundantly consumed during the all year. The
ingestion of the remaining items was highly seasonal. The bivalves were mainly consumed
during the autumn and winter, mysids mostly in summer and autumn and copepods almost
exclusively in the spring, following their highest natural abundance’s in the study areas. The high
number of copepods ingested during that season was also due to the abundant presence of
small juveniles of P. microps in the area in this period.
Juveniles of P. microps increase their niche width as they grew (Thorman, 1983). The main
preys of the smallest size classes (I and II) were epibenthic copepods, while mysids represent a
secondary prey. With the growth of this goby dimension, it was observed a decrease in the
importance of this prey and an increase in the consumption of all the other preys, most of them
endobenthic. Thus, in the following size classes (III and IV), while the mysids maintained their
importance, polychaetes began to be the main item ingested and bivalves were mostly important
as biomass.
For classes V, VI and VII, the annelids were the preferential preys, with an increasing
consumption of bivalves. This prey was the main taxon ingested by the biggest individuals
caught (³ 50mm). The high abundance in the consumption of a larger number of taxa suggests
that the individuals of this late size class explore a more wide trophic niche.
The reduced number of preys and the high percentage of empty guts in the analysis of the
individuals captured on the mouth of the creek during flood suggests that this goby feeds almost
exclusively on the items available inside the creeks. This fact is corroborated by the presence of
a clean fish vertebral column inside one of those guts.
The anterior position of the mysids and bivalves in the digestive track suggests that these preys
are preferentially ingested in the final period of permanency in the creeks while polychaetes and
oligochaetes are mainly ingested in the upper areas of the salt marsh creeks or by the time they
arrive there.
5.2
Food habits of Liza ramada (Risso, 1826) in the Tagus salt marsh
5.2.1
Introdution
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The thin-lipped grey mullet (Liza ramada Risso, 1826) is one of the most successful inshore
teleost fish that inhabit Portuguese waters (Almeida, 1996). In the Tagus estuary is one of the
most common and abundant mugilids.
Feeding directly on the energy produced by the first level of the food web, they avoid the
competition with other trophic groups and have a large contribute on the optimisation of the
energy transference processes (Odum, 1970).
The feeding strategies of this species in the Tagus estuary were already investigated by Almeida
(1996). Nevertheless, there is no information on the importance of the salt marsh for the feeding
ecology of this mugilid and on their roll on the transference of organic matter from these highly
productive areas to the subtidal areas of the estuary.
5.2.2
Methods
Samples of L. ramada were collected in May/June in Hortas salt marsh creek, using the same
methodologies applied for P. microps. Samples were done during flood and ebb tides in order to
compare the food intake before and after residence in salt marshes. The samples were collected
in consecutive days, with tide of the same amplitude.
In the laboratory total length was measured to the nearest 1mm, wet weight was determined to
the nearest 0.0001g and the contents of the cardiac region of the stomach was removed and
weighted to the nearest 0.0001g (stomach content wet weight). A 200mg sample was removed
from each stomach, and suspended in 5 ml of distilled water. The samples were shaken
thoroughly and a known volume pipetted onto a slide with an etched grid. A constant area was
examined in all the samples and the food items found in it were, wherever possible, identified to
the genus level and counted. The identification and counting were made using a stereo
microscope at x 400 magnification.
Determination of the percentage of organic matter in the stomach contents was derived from loss
on ignition at 480ºC after 24h.
The fullness index, the frequency of occurrence, the numerical frequency of each food item and
the vacuity index were estimated according to Hureau (1970).
5.2.3
Results and discussion
The analysis of the stomach contents of L. ramada (table XI) showed the presence of high
quantities of sediment, being identified 18 taxa. The most important taxa ingested by this mugilid
were the diatoms, while nematoda, foraminifera and copepoda were only taken occasionally. The
most abundant food items were Gyrosigma sp. + Pleurosigma sp. and Navicula sp., representing
together more than 80% of the total number of individuals identified. Almeida et al. (1993)
obtained for Alcochete, in the Tagus estuary, similar results.
Table XI. Food items identified in the stomach contents of L. ramada.
Coscinodiscaceae
Ciclotella sp.
Coscinodiscus sp.
Melosira sp.
Actinodiscaceae
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Actinoptychus sp.
Diatomaceae
Fragillaria sp.
Achnanthaceae
Achnanthes sp.
Cocconeis sp.
Naviculaceae
Diploneis sp.
Gyrosigma sp.
Pleurosigma sp.
Navicula sp.
Stauroneis sp.
Nitzschiaceae
Nitzschia sp.
Surirellaceae
Surirella sp.
Desmidiaceae
Closterium sp.
Foraminifera
Nematoda
Copepoda
None of the stomachs analysed was empty.
The analysis of fullness index of the individuals sampled at the moment that the water arrives
into the creeks (table XII) showed that at their arrived into the mouth of the creek their stomach
content represents near 0.77% of their weight. However, when the same analysis was made to
the individuals caught 30 min after high tide, their stomach contents represents 11.40% of their
weight. In the following periods of 30 minutes this value decreases gradually, until 4.85% two
hours after high tide.
Table XII. Fullness index and % of organic matter of L. ramada by the time the flood arrives in
to the creeks and in intervals of 30 min. after high tide.
Time
Nº ind.
Fullness
index
Standard
deviation
%
organic
matter
Standard
deviation
Flood
45
0.77
0.45
9.02
3.10
30 min
13
11.40
3.83
10.63
0.87
60 min
13
9.72
2.87
11.64
1.28
90 min
16
6.22
4.06
11.57
1.47
120 min
4
4.85
2.93
11.90
1.61
In this area L. ramada feeds on the extensive surface of the mudflat areas that becomes
accessible to the mullet only with the rising time that they follow, as observed by Almeida et al.
(1993). Nevertheless, the period of highest ingestion begins by the time they arrive into the
creeks until 1/2 hour after high tide. After this period of intense grazing activity they stop feeding
and return to deepest waters. This fact is confirmed by the highest densities of L. ramada
obtained for the first 1/2 hour of ebb tide, diminishing the risk of stranding inside the creek.
A possible reason for that feeding behaviour could be associated with the higher densities of
microphytobenthos inside the creeks (pers. obs.). The comparison between the percentages of
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organic matter of the stomach contents of the individuals that feed outside with those that feed
inside the creeks, show higher values for the latest ones confirming the presence of higher food
availability inside the creeks.
The total biomass of L. ramada present in the creek during one tide, of the same month, was
246 503.69 g. Thus, it is possible to estimate in more than 25 Kg per tide the amount of material
transported by this species from the salt marsh towards other estuarine areas.
However, these results need to be confirmed with more samples in order to exclude the
hipothesys that the individuals caught during the flood tides were not actively feeders during that
tide.
5.3
Isotope analysis
Based on the first part of the work, biological characterization of the area, and on the literature
available k-species were selected (Tab. XIII) as representative of the different levels of the food
web in the Tagus estuary. Multiple stable isotope analysis (C
13
/ C
12
, S
34
/ S
32
, N
15
/ N
14
) of
those taxa were used for the identification of the different pathways of the Tagus salt marsh food
web.
Table XIII - List of the species representative of the different levels of the food web in the Tagus
salt marsh
Flora
Microphytobenthos
Macrophytes
Spartina maritima
Arthrocnemon fruticuosum
Halimione portulacoides
Fauna
Polichaeta
Hediste diversicolor
Streblospio shrubsolii
Oligochaeta
Oligochaeta n.i.
Gastropoda
Peringia ulvae
Bivalvia
Scrobicularia plana
Isopoda
Cyathura carinata
Sphaeroma serratum
Amphipoda
Orchestia gammarela
Copepoda
Copepoda n.i.
Misidacea
Neomysis integer
Decapoda
Palaemonetes varians
Crangon crangon
Pisces
Liza ramada
Pomatoschistus microps
Sardina pilchardus
5.3.1
Methods
Samples for stable isotope analysis were collected during Spring, due to the higher availability of
the taxa sellected, in two salt marsh tidal creeks, Hortas and Vasa sacos. The preparation of the
samples for isotope analysis was similar as described for the identification of the main sources of
organic matter. For the fish species Pomatoschistus microps and Liza ramada different size
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classes were used for comparison with the results obtained in the gut contents analysis. Two
classes for P. microps (juveniles and adults) and three for L. ramada (juveniles < 50 mm,
juveniles > 50 mm and adults ).
5.3.2
Results
Due to problems in the mass spectrometer only a small part of the results are available, not
allowing any kind of analysis. The
13
C/
12
C isotopic values available are represented in table
XIV. We are expecting at any time the rest of the C results, as well as those of N and S.
Table XIV - Isotopic values (‰ ) of
13
C/
12
C available for both sites Hortas and Vasa sacos.
Taxa
Hortas
Vasa sacos
Scrobicularia plana (bivalvae)
-19.17
-15.86
Oligochaeta
-
-15.20
Capitelidae (polychaeta)
-16.69
-
Hediste diversicolor (polychaeta)
-16.31
-
Sphaeroma monodi (isopoda)
-
-18.93
Orchestia gammarela (amphipoda)
-17.17
-
Peringia ulvae (gastropoda)
-16.31
-16.16
Palaemonetes varians (decapoda)
-17.06
-17.46
Pomatoschistus microps adult (pisces)
-16.04
-15.96
Liza ramada small juvenile (pisces)
-17.95
-17.90
Liza ramada big juvenile (pisces)
-14.05
-14.21
Liza ramada adult (pisces)
-
-16.35
5.4
Food web
The food web of the upper Tagus estuary (including subtidal and lower intertidal areas) and of the
salt marsh/mud flat areas (medium and upper intertidal areas) is represented respectively in
figures 20 and 21. In those diagrams are present the most abundant taxa present in the areas
representative of the different levels of the food web.
In the first areas the plant biomass, mainly from riverine inputs, microalgae and salt marsh
species, is decomposed and enters the detritus pathway. Microbial fungi and bacteria are
primary consumers wich are preyed by small crustaceans, as the amphipod Corophium
volutator. Bacteria, fungi and detritus were considered in the same group.
As deposit feeders there is a high abundance of oligochaetes and polychaetes (mainly spionidae
and Hedistes diversicolor). According to Silva (1993) the rag worm H. diversicolor consumes
mostly inorganic and decomposed organic matter, although the ingestion of microalgae and some
benthic invertebrates also occurs. This species seems to adopt an omnivorous diet with
detritivorous predominance, emerging from his tube to feed on the surface
The gastropod Peringia ulvae is a deposit feeder that also grazes on the benthic microalgae.
A large population of the bivalve peppery furrow shell (Scrobicularia plana), are present in these
areas. Being a detritus feeder this species suck the detritus from the mud surface using the
inhalant siphon and vacuum-cleaning the substratum.
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The green crab Carcinus maenas is an omnivorous species that feeds on a large spectrum of
death and living preys. According to Martins (1995) the main items ingested by this species are
fish (especially gobies), shrimps, small crustaceans and polychaetes, as H. diversicolor.
The brown shrimp Crangon crangon, the most abundant natantia in the area, has as preferential
food items polychaetes and small crustaceans, but they also prey on bivalves and small fishes
(Pomatoschistus spp.). Being a generalist, the ingestion of the different preys is dependent on
their abundance (Martins, 1995).
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The estuarine resident fish are represented by 4 species. The common goby Pomatoschistus
microps and the sand goby P. minutus feed mainly on polychaetes, oligochaetes, bivalve
siphons and small crustaceans, such as copepods, mysids, amphipods, isopods and shrimps.
Canibalism was also observed for both species (Salgado, 1995).
The pipe-fish Syngnathus sp. and the european anchovy Engraulis encrasicolus are
planktivorous species, ingesting preferentially mysids.
Two catadromous migratory species occur in these areas. The common eel Anguilla anguilla
according to Costa et al. (1992) ingests green crabs Carcinus maenas and fishes as preferential
and secondary food sources. However, shrimps and amphipods are also important items on this
species diet.
The thin-lipped grey mullet Liza ramada, is one of the most common species in the area, being
the most abundant in terms of biomass. This species is a detritus feeder grazing on the
extensive mudflat areas where they ingest high quantities of benthic microalgae such as
Bacilliarophycea, Cyanophycea, Zygophycea and a large amount of detritus (Almeida, 1996).
These upper areas are used as nursery by mainly three fish species, two soles Solea solea
(common sole) and Solea senegalensis (Senegal sole) and the sea bass Dicentrarchus labrax.
The diet of the soles is mainly composed of polychaetes (especially spionidae and H.
diversicolor) and amphipods (Corophium volutator) (Cabral, 1998). According to that author the
main difference on both species diet is the higher amount of bivalves consumed by S.
senegalensis.
The diet of the young sea bass is mainly based on the ingestion of crustaceans, such as
decapods (mainly shrimps), mysids and amphipods (Corophium volutator).
The Tagus estuary has very important wintering populations of several shore bird species,
mainly herons, flamingos, gulls and ducks, which use the intertidal areas as feeding grounds. It
is also the most important site for wintering waders in the country.
According to Moreira (1995) heron’s prey on small fish and decapod crustaceans such as the
brown shrimp and the green crab. The gulls in the area feed mostly on bivalves (Scrobicularia
plana) and polychaetes (mainly H. diversicolor), eating also crustaceans.
The diet of the waders inclued oligochaetes, polychaetes, the gastropode P. ulvae and the
bivalve S. plana, which is ingested as siphons or as the whole individual. Moreira (1995) found
that this last item represents a significant percentage of biomass removed by the bird population.
Comparativelly, in the salt marsh/mud flat food web (figure 21) there is a higher contribution of
the salt marsh plants for the total plant biomass available for the first consumers.
The abundance of the amphipod C. volutator and the shrimp C. crangon are very reduced in the
salt marsh. However, their niche is occupied by the isopod Sphaeroma monodi and by the
shrimp Palaemonetes varians.
Nevertheless, the major difference between both food webs is the absence or presence in lower
abundances of several fish species, as the ell, the sea bass, the sand goby and the soles. Most
of those species are potencial predators of small fish. Thus, young of the year of several fish
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species feeding in the salt marsh areas decrease the risk of being preyed by other fish species.
The reduced presence of the green crab in this area is also a factor contributing to that lower
predation risk.
What concerns the birds, the presence of flamingos and ducks is restricted to the salt marsh and
the close mud flat areas (Moreira, 1995). The ducks eat salt marsh vegetation, while the
flamingos use the intertidal areas adjacent to the salt marsh to feed on small invertebrates.
6
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7
PUBLICATIONS
This task enabled the publication or the submission of four articles:
Cabral H.N. and Costa M.J. (1999). Differential use of nursery areas within the Tagus estuary by
sympatric soles, Solea solea and Solea senegalensis. Env. Biol. Fishes, 56 : 389-397.
Costa M.J. and Cabral H.N. (1999). Changes in the Tagus nursery function for commercial fish
species: some perspectives for management. Aquatic Ecol., 33 : 287-292.
Serôdio J., da Silva J.M. and Catarino F. -Use of in vivo chlorophyll a fluorescence to quantify
short-term variations in the productive biomass of intertidal microphytobenthos. (Submitted)
Salgado J.P., Cabral H.N.. and Costa M.J.-Comparison of the fish assemblage in the tidal
saltmarsh creeks and in the adjoining mudflat areas in the Tagus estuary. (Submitted)
It was the object of a Phd thesis: by Serôdio J. (1999)
Modelling the primary productivity of intertidal microphytobenthos. Role of migratory rhythms
studied by in vivo chlorophyill a fluorometry. PhD Thesis, University of Lisboa (Portugal).
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